Neurodynamics and Causality 1 Walter J Freeman
Consciousness, Intentionality, and Causality
Walter J Freeman
Department of Molecular & Cell Biology, LSA 129
University of California at Berkeley CA 94720-3200
TEL 510-642-4220 FAX 510-643-6791
wfreeman@socrates.berkeley.edu
Journal of Consciousness Studies 6 Nov/Dec: 143-172, 1999
Key words: awareness, causality, consciousness, emotion,
intentionality, nonlinear dynamics, reafference, self-control
Running Title: Neurodynamics and Causality
Abstract
To explain how stimuli cause consciousness, we have to explain causality. We
can't trace linear causal chains from receptors after the first cortical synapse, so
we use circular causality to explain neural pattern formation by self-organizing
dynamics. But an aspect of intentional action is causality, which we extrapolate
to material objects in the world. Thus causality is a property of mind, not matter.
Summary
1 According to behavioral theories deriving from pragmatism, Gestalt
psychology, existentialism, and ecopsychology, knowledge about the world is
gained by intentional action followed by learning. In terms of the
neurodynamics described here, if the intending of an act comes to awareness
through reafference, it is perceived as a cause. If the consequences of an act
come to awareness through proprioception and exteroception, they are
perceived as an effect. A sequence of such states of awareness comprises
consciousness, which can grow in complexity to include self-awareness.
Intentional acts do not require awareness, whereas voluntary acts require self-
awareness. Awareness of the action/perception cycle provides the cognitive
metaphor of linear causality as an agency. Humans apply this metaphor to
objects and events in the world to predict and control them, and to assign social
responsibility. Thus linear causality is the bedrock of social contracts and
technology.
2 Complex material systems with distributed nonlinear feedback, such as
brains and their neural and behavioral activities, cannot be explained by linear
causality. They can be said to operate by circular causality without agency.
The nature of self-control is described by breaking the circle into a forward limb,
the intentional self, and a feedback limb, awareness of the self and its actions.
The two limbs are realized through hierarchically stratified kinds of neural
activity. Actions are governed by the self-organized microscopic neural activity
of cortical and subcortical components in the brain. Awareness supervenes as
Neurodynamics and Causality 2 Walter J Freeman
a macroscopic ordering state, that defers action until the self-organizing
microscopic process has reached a closure in reflective prediction. Agency,
which is removed from the causal hierarchy by the appeal to circularity, re-
appears as a metaphor by which events in the world are anthropomorphized,
making them subject to the illusion of human control.
1. Introduction
3 What is consciousness? It is known through experience of the activities of
one's own body and observation of the bodies of others. In this respect the
question whether it arises from the soul (Eccles, 1994), or from panpsychic
properties of matter (Whitehead, 1938; Penrose, 1994; Chalmers, 1996), or as a
function of brain operations (Searle, 1992; Dennett, 1991; Crick, 1994) is not
relevant. The pertinent questions are - however it arises and is experienced -
how and in what senses does it cause the functions of brains and bodies, and
how do brain and body functions cause it? How do actions cause perceptions;
how do perceptions cause awareness; and how do states of awareness cause
actions? Analysis of causality is a necessary step toward a comprehension of
consciousness, because the forms of answers depend on the choice among
meanings that are assigned to "cause": (a) to make, move and modulate (an
agency in linear causality); (b) to explain, rationalize and blame (cognition in
circular causality without agency but with top-down-bottom-up interaction); or (c)
to flow in parallel as a meaningful experience, by-product, or epiphenomenon
(noncausal interrelation).
4 The elements of linear causality (a) are shown in Figure 1 in terms of
stimulus-response determinism. A stimulus initiates a chain of events including
activation of receptors, transmission by serial synapses to cortex, integration
with memory, selection of a motor pattern, descending transmission to motor
neurons, and activation of muscles. At one or more nodes along the chain,
awareness occurs, and meaning and emotion are attached to the response.
Temporal sequencing is crucial; no effect can precede or occur simultaneously
with its cause. At some instant each effect becomes a cause. The
demonstration of causal invariance must be based on repetition of trials. The
time line is reinitiated at zero in observer time, and S-R pairs are collected.
Some form of generalization is used. In the illustration it is by time ensemble
averaging. Events with small variance in time of onset close to stimulus arrival
are retained. Later events with varying latencies are lost. The double dot
indicates a point in real time; it is artificial in observer time. This
conceptualization is inherently limited, because awareness cannot be defined
at a point in time.
5 The elements of circular causality (b) are shown in Figure 2. The double dot
shows a point moving counterclockwise on a trajectory idealized as a circle, in
order to show that an event exists irresolvably as a state through a period of
inner time, which we reduce to a point in real time. Stimuli from the world
impinge on this state. So also do stimuli arising from the self-organizing
dynamics within the brain. Most stimuli are ineffective, but occasionally one
Neurodynamics and Causality 3 Walter J Freeman
succeeds as a "hit" on the brain state, and a response occurs. The impact and
motor action are followed by a change in brain structure that begins a new orbit.
Neurodynamics and Causality 4 Walter J Freeman
LIN EA R CA USA LITY O F TH E O BSERV ER
stim uli responses
causalchain
...
S1 R1
S2 R2
averaging
Sn Rn
0 observer tim e tn
Figure 1. Linear causality is the view of connected events by which causal
chains are constructed. The weaknesses lie in requirements to assign points in
time to the beginning and the end of each chain, and to intervening events in
the chain in strict order, and to repeat pairs of observations in varying
circumstances in order to connect pairs of classes of events. As Davidson
(1980) remarked, events have causes; classes have relations. In the example,
analysis of stimulus-dependent events such as evoked potentials is done by
time ensemble averaging, which degrades nonsynchronized events, and which
leads to further attempts at segmentation in terms of the successive peaks, thus
losing sight of an event extended in time. The notion of 'agency' is implicit in
each event in the chain acting to produce an effect, which then becomes the
next cause.
Neurodynamics and Causality 5 Walter J Freeman
CIRCULA R CA USA LITY O F THE SELF
birth outer
stim uli, S
inner
tim e death
tim e
lim bic
activity =
inner stim uli
“hits” = real
responses,R
Figure 2. Circular causality expresses the interrelations between levels in a
hierarchy: a top-down macroscopic state simultaneously influences microscopic
particles that bottom-up create and sustain the macroscopic state. The state
exists over a span of inner time in the system that can be collapsed to a point in
external time. Events in real time are marked by changes in the state of the
system, which are discrete. This conceptualization is widely used in the social
and physical sciences. In an example used by Haken (1983), the excited atoms
in a laser cause coherent light emission, and the light imposes order on the
atoms. The laser was also used by Cartwright (1989) to exemplify levels of
causality, by which she contrasted simple, direct cause-effect relations not
having significant interactions or second-order perturbations with higher order
"capacities" (according to her, closely related to Mill's "tendencies", but differing
by "material abstraction", p. 226), which by virtue of abstraction have an
enlarged scope of forward action, but which lack the circular relation between
microscopic and macroscopic entities that is essential for explaining lasers -
and brains. The notion of an 'agency' does not enter, and multiple scales of
time and space are required for the different levels.
Neurodynamics and Causality 6 Walter J Freeman
A succession of orbits can be conceived as a cylinder with its axis in real time,
extending from birth to death of an individual and its brain. Events are
intrinsically not reproducible. Trajectories in inner time may be viewed as
fusing past and future into an extended present by state transitions. The circle
is a candidate for representing a state of awareness.
6 Noncausal relations (c) are described by statistical models, differential
equations, phase portraits, and so on, in which time may be implicit or
reversible. Once the constructions are completed by the calculation of risk
factors and degrees of certainty from distributions of observed events and
objects, the assignment of causation is optional. In describing brain functions
awareness is treated as irrelevant or epiphenomenal.
7 These concepts are applied to animal consciousness on the premiss that the
structures and activities of brains and bodies are comparable over a broad
variety of animals including humans. The hypothesis is that the elementary
properties of consciousness are manifested in even the simplest of extant
vertebrates, and that structural and functional complexity increases with the
evolution of brains into higher mammals. The dynamics of simpler brains is
described in terms of neural operations that provide goal-oriented behavior.
In the first half of this essay (Sections 2-6) I describe the neural mechanisms of
intention and reafference and learning, as I see them. I compare explanations
of neural mechanisms using linear and circular causality at three levels of
hierarchical function. In the second half I describe some applications of this
view in the fields of natural sciences. The materials I use to answer the
question, what is causality?, come from several disciplines, including heavy
reliance on neurobiology and nonlinear dynamics. In the words of computer
technologists these two disciplines make up God's own firewall, which keeps
hackers from burning in to access and crack the brain codes. For reviews on
neuroflaming I recommend introductory texts by Bloom and Lazerson (1988) on
"Brain, Mind and Behavior", and by Abraham et al. (1990) on "Visual
Introduction to Dynamical Systems Theory for Psychology."
2. Level 1: The circular causality of intentionality
8 An elementary process requiring the dynamic interaction between brain,
body and world in all animals is an act of observation. This is not a passive
receipt of information from the world, as expressed implicitly in Figure 1. It is the
culmination of purposive action by which an animal directs its sense organs
toward a selected aspect of the world and abstracts, interprets, and learns from
the resulting sensory stimuli (Figure 2). The act requires a prior state of
readiness that expresses the existence of a goal, a preparation for motor action
to position the sense organs, and selective sensitization of the sensory cortices.
Their excitability has already been shaped by the past experience that is
relevant to the goal and the expectancy of stimuli. A concept that can serve as a
principle by which to assemble and interrelate these multiple facets is
intentionality. This concept has been used in different contexts, since its
synthesis by Aquinas (1272) 700 years ago. The properties of intentionality as
Neurodynamics and Causality 7 Walter J Freeman
it is developed here are (a) its intent or directedness toward some future state or
goal; (b) its unity; and (c) its wholeness (Freeman 1995).
9 (a) Intent comprises the endogenous initiation, construction, and direction of
behavior into the world, combined with changing the self by learning in
accordance with the perceived consequences of the behavior. Its origin lies
within brains. Humans and other animals select their own goals, plan their own
tactics, and choose when to begin, modify, and stop sequences of action.
Humans at least are subjectively aware of themselves acting. This facet is
commonly given the meaning of purpose and motivation by psychologists,
because, unlike lawyers, they usually do not distinguish between intent and
motive. Intent is a forthcoming action, and motive is the reason.
10 (b) Unity appears in the combining of input from all sensory modalities into
Gestalten, in the coordination of all parts of the body, both musculoskeletal and
autonomic, into adaptive, flexible, yet focused movements, and in the full weight
of all past experience in the directing of each action. Subjectively, unity may
appear in the awareness of self. Unity and intent find expression in modern
analytic philosophy as "aboutness", meaning the way in which beliefs and
thoughts symbolized by mental representations refer to objects and events in
the world, whether real or imaginary. The distinction between inner image and
outer object calls up a dichotomy between subject and object that was not part
of the originating Thomistic view.
11 (c) Wholeness is revealed by the orderly changes in the self and its
behavior that constitute the development and maturation of the self through
learning, within the constraints of its genes and its material, social and cultural
environments. Subjectively, wholeness is revealed in the striving for the
fulfillment of the potential of the self through its lifetime of change. Its root
meaning is "tending", the Aristotelian view that biology is destiny. It is also seen
in the process of healing of the brain and body from damage and disruption.
The concept appears in the description by a 14th century surgeon, LaFranchi of
Milan, of two forms of healing, by first intention with a clean scar, and by second
intention with suppuration. It is implicit in the epitaph of Ambroise Paré, 16th
century French surgeon: "Je le pansay, Dieu le guarit" (I bound his wounds,
God healed him). Pain is intentional in that it directs behavior toward facilitation
of healing, and that it mediates learning when actions have gone wrong with
deleterious, unintended consequences. Pain serves to exemplify the
differences between volition, desire and intent; it is willed by sadists, desired by
masochists, and essential for normal living.
12 Intentionality cannot be explained by linear causality, because actions
under that concept must be attributed to environmental (Skinner, 1969) and
genetic determinants (Herrnstein and Murray, 1994), leaving no opening for
self-determination. Acausal theories (Hull, 1943; Grossberg, 1982) describe
statistical and mathematical regularities of behavior without reference to
intentionality. Circular causality explains intentionality in terms of "action-
perception cycles" (Merleau-Ponty, 1945) and affordances (Gibson, 1979), in
which each perception concomitantly is the outcome of a preceding action and
Neurodynamics and Causality 8 Walter J Freeman
the condition for a following action. Dewey (1914) phrased the same idea in
different words; an organism does not react to a stimulus but acts into it and
incorporates it. That which is perceived already exists in the perceiver, because
it is posited by the action of search and is actualized in the fulfillment of
expectation. The unity of the cycle is reflected in the impossibility of defining a
moving instant of 'now' in subjective time, as an object is conceived under
linear causality. The Cartesian distinction between subject and object does not
appear, because they are joined by assimilation in a seamless flow.
3. Level 2: The circular causality of reafference
13 Brain scientists have known for over a century that the necessary and
sufficient part of the vertebrate brain to sustain minimal intentional action, a
component of intentionality, is the ventral forebrain, including those parts that
comprise the external shell of the phylogenetically oldest part of the forebrain,
the paleocortex, and the underlying nuclei such as the amydala with which the
cortex is interconnected. These components suffice to support identifiable
patterns of intentional behavior in animals, when all of the newer parts of the
forebrain have been surgically removed (Goltz, 1892) or chemically inactivated
by spreading depression (Bures et al., 1974). Intentional behavior is severely
altered or lost following major damage to these parts. Phylogenetic evidence
comes from observing intentional behavior in salamanders, which have the
simplest of the existing vertebrate forebrains (Herrick, 1948; Roth, 1987)
comprising only the limbic system. Its three cortical areas are sensory (which is
predominantly the olfactory bulb), motor (the pyriform cortex), and associational
(Figure 3). The latter has the primordial hippocampus connected to the septal,
amygdaloid and striatal nuclei. It is identified in higher vertebrates as the locus
Neurodynamics and Causality 9 Walter J Freeman
Figure 3. The schematic shows the dorsal view of the right cerebral hemisphere
of the salamander (adapted from Herrick 1948). The unbroken sheet of
superficial neuropil sustains bidirectional interactions between all of its parts,
which are demarcated by their axonal connections with sensory receptors
(olfactory bulb and 'Transitional zone' for all other senses, descending
connections to the corpus striatum, amygdaloid and septum from the pyriform
area, and the intrinsic connections between these areas and the primordial
hippocampus posteromedially. This primitive forebrain suffices as an organ of
intentionality, comprising the limbic system with little else besides.
Neurodynamics and Causality 10 Walter J Freeman
of the functions of spatial orientation (the "cognitive map") and temporal
orientation in learning ("short term memory"). These integrative frameworks are
essential for intentional action into the world, because even the simplest
actions, such as observation, searching for food or evading predators, require
an animal to coordinate its position in the world with that of its prey or refuge,
and to evaluate its progress during evaluation, attack or escape .
14 The crucial question for neuroscientists is, how are the patterns of neural
activity that sustain intentional behavior constructed in brains? A route to an
answer is provided by studies of the electrical activity of the primary sensory
cortices of animals that have been trained to identify and respond to
conditioned stimuli. An answer appears in the capacity of the cortices to
construct novel patterns of neural activity by virtue of their self-organizing
dynamics.
15 Two approaches to the study of sensory cortical dynamics are in contrast.
One is based in linear causality (Figure 1). An experimenter identifies a neuron
in sensory cortex by recording its action potential with a microelectrode, and
then determines the sensory stimulus to which that neuron is most sensitive.
The pulse train of the neuron is treated as a symbol to 'represent' that stimulus
as the 'feature' of an object, for example the color, contour, or motion, of an eye
or a nose in a face. The pathway of activation from the sensory receptor
through relay nuclei to the primary sensory cortex and then beyond is described
as a series of maps, in which successive representations of the stimulus are
activated. The firings of the feature detector neurons must then be
synchronized or 'bound' together to represent the object, such as a moving
colored ball, as it is conceived by the experimenter. This representation is
thought to be transmitted to a higher cortex, where it is compared with
representations of previous objects that are retrieved from memory storage. A
solution to the 'binding problem' is still being sought (Gray, 1994; Hardcastle,
1994; Singer and Gray, 1995).
16 The other approach is based in circular causality (Figure 2). In this view the
experimenter trains a subject to cooperate through use of positive or negative
reinforcement, thereby inducing a state of expectancy and search for a stimulus,
as it is conceived by the subject. When the expected stimulus arrives, the
activated receptors transmit pulses to the sensory cortex, where they elicit the
construction by nonlinear dynamics of a macroscopic, spatially coherent
oscillatory pattern that covers the entire cortex (Freeman, 1975, 1991). It is
observed by means of the electroencephalogram (EEG) from electrode arrays
on all the sensory cortices (Freeman, 1975, 1992, 1995; Barrie et al., 1996; Kay
and Freeman 1998). It is not seen in recordings from single neuronal action
potentials, because the fraction of the variance in the single neuronal pulse
train that is covariant with the neural mass is far too small, on the order of 0.1%.
17 The emergent pattern is not a representation of a stimulus, nor a ringing as
when a bell is struck, nor a resonance as when one string of a guitar vibrates
when another string does so at its natural frequency. It is a phase transition that
is induced by a stimulus, followed by a construction of a pattern that is shaped
Neurodynamics and Causality 11 Walter J Freeman
by the synaptic modifications among cortical neurons from prior learning. It is
also dependent on the brain stem nuclei that bathe the forebrain in
neuromodulatory chemicals. It is a dynamic action pattern that creates and
carries the meaning of the stimulus for the subject. It reflects the individual
history, present context, and expectancy, corresponding to the unity and the
wholeness of intentionality. Owing to dependence on history, the patterns
created in each cortex are unique to each subject.
18 The visual, auditory, somesthetic and olfactory cortices serving the distance
receptors all converge their constructions through the entorhinal cortex into the
limbic system, where they are integrated with each other over time. Clearly they
must have similar dynamics, in order that the messages be combined into
Gestalten. The resultant integrated meaning is transmitted back to the cortices
in the processes of selective attending, expectancy, and the prediction of future
inputs (Freeman, 1995; Kay and Freeman, 1998).
19 The same wave forms of EEG activity as those found in the sensory cortices
are found in various parts of the limbic system. This similarity indicates that the
limbic system also has the capacity to create its own spatiotemporal patterns of
neural activity. They are embedded in past experience and convergent
multisensory input, but they are self-organized. The limbic system provides
interconnected populations of neurons, that, according to the hypothesis being
proposed, generate continually the patterns of neural activity that form goals
and direct behavior toward them.
20 EEG evidence shows that the process in the various parts occurs in
discontinuous steps (Figure 2), like frames in a motion picture (Freeman, 1975;
Barrie, Freeman and Lenhart, 1996). Being intrinsically unstable, the limbic
system continually transits across states that emerge, transmit to other parts of
the brain, and then dissolve to give place to new ones. Its output controls the
brain stem nuclei that serve to regulate its excitability levels, implying that it
regulates its own neurohumoral context, enabling it to respond with equal
facility to changes, both in the body and the environment, that call for arousal
and adaptation or rest and recreation. Again by inference it is the
neurodynamics of the limbic system, with contributions from other parts of the
forebrain such as the frontal lobes and basal ganglia, that initiates the novel
and creative behavior seen in search by trial and error.
21 The limbic activity patterns of directed arousal and search are sent into the
motor systems of the brain stem and spinal cord (Figure 4). Simultaneously,
patterns are transmitted to the primary sensory cortices, preparing them for the
consequences of motor actions. This process has been called "reafference"
(von Holst and Mittelstädt 1950; Freeman 1995), "corollary discharge" (Sperry
1950), "focused arousal", and "preafference" (Kay and Freeman, 1998). It
compensates for the self-induced changes in sensory input that accompany the
actions organized by the limbic system, and it sensitizes sensory systems to
anticipated stimuli prior to their expected times of arrival.
Neurodynamics and Causality 12 Walter J Freeman
Figure 4. In the view of dynamics the limbic architecture is formed by multiple
loops. The mammalian entorhinal cortex is the target of convergence of all
sensory input, the chief source of input for the hippocampus, its principal target
for its output, and a source of centrifugal input to all of the primary sensory
cortices. The hypothesis is proposed that intentional action is engendered by
counterclockwise flow of activity around the loops into the body and the world,
comprising implicit cognition, and that awareness and consciousness are
engendered by clockwise flow within the brain, comprising explicit cognition.
The intentional flow consists in the microscopic activity of brain subsystems, and
the back flow is the macroscopic order parameter that by circular causality
regulates and holds or releases the activity of the subsystems.
Neurodynamics and Causality 13 Walter J Freeman
22 The concept of preafference began with an observation by Helmholtz (1872)
on patients with paralysis of lateral gaze, who, on trying and being unable to
move an eye, reported that the visual field appeared to move in the opposite
direction. He concluded that "an impulse of the will" that accompanied
voluntary behavior was unmasked by the paralysis. He wrote: "These
phenomena place it beyond doubt that we judge the direction of the visual axis
only by the volitional act by means of which we seek to alter the position of the
eyes.". J. Hughlings Jackson (1931) repeated the observation, but postulated
alternatively that the phenomenon was caused by "an in-going current", which
was a signal from the non-paralyzed eye that moved too far in the attempt to
fixate an object, and which was not a recursive signal from a "motor centre". He
was joined in this interpretation by William James (1893) and Edward Titchener
(1907), thus delaying deployment of the concepts of neural feedback in re-
entrant cognitive processes until late in the 20th century.
23 The sensory cortical constructions consist of brief staccato messages to the
limbic system, which convey what is sought and the result of the search. After
multisensory convergence, the spatiotemporal activity pattern in the limbic
system is up-dated through temporal integration in the hippocampus.
Accompanying sensory messages there are return up-dates from the limbic
system to the sensory cortices, whereby each cortex receives input that has
been integrated with the input from all others, reflecting the unity of
intentionality. Everything that a human or an animal knows comes from the
circular causality of action, preafference, perception, and up-date. It is done by
successive frames of self-organized activity patterns in the sensory and limbic
cortices.
4. Level 3: Circular causality among neurons and neural masses
24 The "state" of the brain is a description of what it is doing in some specified
time period. A phase transition occurs when the brain changes and does
something else. For example, locomotion is a state, within which walking is a
rhythmic pattern of activity that involves large parts of the brain, spinal cord,
muscles and bones. The entire neuromuscular system changes almost
instantly with the transition to a pattern of jogging or running. Similarly, a
sleeping state can be taken as a whole, or divided into a sequence of slow
wave and REM stages. Transit to a waking state can occur in a fraction of a
second, whereby the entire brain and body shift gears, so to speak. The state of
a neuron can be described as active and firing or as silent, with sudden
changes in patterns of firing constituting phase transitions. Populations of
neurons also have a range of states, such as slow wave, fast activity, seizure, or
silence. The science of dynamics describes states and their phase transitions.
25 The most critical question to ask about a state is its degree of stability or
resistance to change. Stability is evaluated by perturbing an object or a system
(Freeman 1975). For example, an egg on a flat surface is unstable, but a coffee
mug is stable. A person standing on a moving bus and holding on to a railing is
stable, but someone walking in the aisle is not. If a person regains his chosen
Neurodynamics and Causality 14 Walter J Freeman
posture after each perturbation, no matter in which direction the displacement
occurred, that state is regarded as stable, and it is said to be governed by an
attractor. This is a metaphor to say that the system goes (" is attracted to") the
state through interim transiency. The range of displacement from which
recovery can occur defines the basin of attraction, in analogy to a ball rolling to
the bottom of a bowl. If a perturbation is so strong that it causes concussion or a
broken leg, and the person cannot stand up again, then the system has been
placed outside the basin of attraction, and a new state supervenes with its own
attractor and basin of attraction.
26 Stability is always relative to the time duration of observation and the criteria
for what is chosen to be observed. In the perspective of a lifetime, brains
appear to be highly stable, in their numbers of neurons, their architectures and
major patterns of connection, and in the patterns of behavior they produce,
including the character and identity of the individual that can be recognized and
followed for many years. A brain undergoes repeated transitions from waking to
sleeping and back again, coming up refreshed with a good night or irritable with
insomnia, but still, giving arguably the same person as the night before. But in
the perspective of the short term, brains are highly unstable. Thoughts go
fleeting through awareness, and the face and body twitch with the passing of
emotions. Glimpses of the internal states of neural activity reveal patterns that
are more like hurricanes than the orderly march of symbols in a computer, with
the difference that hurricanes don't learn. Brain states and the states of
populations of neurons that interact to give brain function, are highly irregular in
spatial form and time course. They emerge, persist for a small fraction of a
second, then disappear and are replaced by other states.
27. Neuroscientists aim to describe and measure these states and tell what they
mean both to observations of behavior and to experiences with awareness. We
approach the dynamics by defining three kinds of stable state, each with its type
of attractor. The simplest is the point attractor. The system is at rest unless
perturbed, and it returns to rest when allowed to do so. As it relaxes to rest, it
has a brief history, but loses it on convergence to rest. Examples of point
attractors are neurons or neural populations that have been isolated from the
brain, and also the brain that is depressed into inactivity by injury or a strong
anesthetic, to the point where the EEG has gone flat. A special case of a point
attractor is noise. This state is observed in populations of neurons in the brain
of a subject at rest, with no evidence of overt behavior or awareness. The
neurons fire continually but not in concert with each other. Their pulses occur in
long trains at irregular times. Knowledge about the prior pulse trains from each
neuron and those of its neighbors up to the present fails to support the
prediction of when the next pulse will occur. The state of noise has continual
activity with no history of how it started, and it gives only the expectation that its
average amplitude and other statistical properties will persist unchanged.
28 A system that gives periodic behavior is said to have a limit cycle attractor.
The classic example is the clock. When it is viewed in terms of its ceaseless
motion, it is regarded as unstable until it winds down, runs out of power, and
goes to a point attractor. If it resumes its regular beat after it is re-set or
Neurodynamics and Causality 15 Walter J Freeman
otherwise perturbed, it is stable as long as its power lasts. Its history is limited to
one cycle, after which there is no retention of its transient approach in its basin
to its attractor. Neurons and populations rarely fire periodically, and when they
appear to do so, close inspection shows that the activities are in fact irregular
and unpredictable in detail, and when periodic activity does occur, it is either
intentional, as in rhythmic drumming, or pathological, as in nystagmus and
Parkinsonian tremor.
29 The third type of attractor gives aperiodic oscillation of the kind that is
observed in recordings of EEGs and of physiological tremors. There is no one
or small number of frequencies at which the system oscillates. The system
behavior is therefore unpredictable, because performance can only be
projected far into the future for periodic behavior. This type was first called
"strange"; it is now widely known as "chaotic". The existence of this type of
oscillation was known to mathematicians a century ago, but systematic study
was possible only recently after the full development of digital computers. The
best known simple systems with chaotic attractors have a small number of
components and a few degrees of freedom, as for example, the double-hinged
pendulum, and the dripping faucet. Large and complex systems such as
neurons and neural populations are thought to be capable of chaotic behavior,
but proof is not yet possible at the present level of developments in
mathematics.
30 The discovery of chaos has profound implications for the study of brain
function (Skarda and Freeman 1987). A dynamic system has a collection of
attractors, each with its basin, which forms an 'attractor landscape' with all three
types. The state of the system can jump from one to another in an itinerant
trajectory (Tsuda 1991). Capture by a point or limit cycle attractor wipes clean
the history upon asymptotic convergence, but capture in a chaotic basin
engenders continual aperiodic activity, thereby creating novel, unpredictable
patterns that retain its history.
31 Although the trajectory is not predictable, the statistical properties such as
the mean and standard deviation of the state variables of the system serve as
measures of its steady state. Chaotic fluctuations carry the system endlessly
around in the basin. However, if energy is fed into the system so that the
fluctuations increase in amplitude, or if the landscape of the system is changed
so that the basin shrinks or flattens, a microscopic fluctuation can carry the
trajectory across the boundary between basins to another attractor. This
crossing constitutes a first order phase transition.
32 In each sensory cortex there are multiple chaotic attractors with basins
corresponding to previously learned classes of stimuli, including that for the
learned background stimulus configuration, which constitutes an attractor
landscape. This chaotic prestimulus state of expectancy establishes the
sensitivity of the cortex by warping the landscape, so that a very small number
of sensory action potentials driven by an expected stimulus can carry the
cortical trajectory into the basin of an appropriate attractor. Circular causality
enters in the following way. The state of a neural population in an area of
Neurodynamics and Causality 16 Walter J Freeman
cortex is a macroscopic event that arises through the interactions of the
microscopic activity of the neurons comprising the neuropil. The global state is
upwardly generated by the microscopic neurons, and simultaneously the global
state downwardly organizes the activities of the individual neurons.
33 Each cortical phase transition requires this circularity. It is preceded by a
conjunction of antecedents. A stimulus is sought by the limbic brain through
orientation of the sensory receptors in sniffing, looking, and listening. The
landscape of the basins of attraction is shaped by limbic preafference, which
facilitates access to an attractor by expanding its basin for the reception of a
desired class of stimuli. Preafference provides the ambient context by
multisensory divergence. The web of synaptic connections modified by prior
learning maintains the basins and attractors. Pre-existing chaotic fluctuations
are enhanced by input, forcing the selection of a new macroscopic state that
then engulfs the stimulus-driven microscopic activity.
34 The first proposed reason that all the sensory systems (visual, auditory,
somatic and olfactory) operate this way is the finite capacity of the brain faced
with the infinite complexity of the environment. In olfaction, for example, a
significant odorant may consist of a few molecules mixed in a rich and powerful
background of undefined substances, and it may be continually changing in
age, temperature, and concentration. Each sniff in a succession with the same
chemical activates a different subset of equivalent olfactory receptors, so the
microscopic input is unpredictable and unknowable in detail. Detection and
tracking require an invariant pattern over trials. This is provided by the attractor,
and the generalization over equivalent receptors is provided by the basin. The
attractor determines the response, not the particular stimulus. Unlike the view
proposed by stimulus-response reflex determinism, the dynamics gives no
linear chain of cause and effect from stimulus to response that can lead to the
necessity of environmental determinism. The second proposed reason is the
requirement that all sensory patterns have the same basic form, so that they can
be combined into Gestalts, once they are converged to be integrated over time.
5. Circular causality in awareness
35 Circular causality, then, occurs with each phase transition in sensory
cortices and the olfactory bulb, when fluctuations in microscopic activity exceed
a certain threshold, such that a new macroscopic oscillation emerges to force
cooperation on the very neurons that have brought the pattern into being. EEG
measurements show that multiple patterns self-organize independently in
overlapping time frames in the several sensory and limbic cortices, coexisting
with stimulus-driven activity in different areas of the neocortex, which structurally
is an undivided sheet of neuropil in each hemisphere receiving the projections
of sensory pathways in separated areas.
36 Circular causality can serve as the framework for explaining the operation of
awareness in the following way. The multimodal macroscopic patterns
converge simultaneously into the limbic system, and the results of integration
over time and space are simultaneously returned to all of the sensory systems.
Neurodynamics and Causality 17 Walter J Freeman
Here I propose that another level of hierarchy exists in brain function as a
hemispheric attractor, for which the local macroscopic activity patterns are the
components. The forward limb of the circle provides the bursts of oscillations
converging into the limbic system that destabilize it to form new patterns. The
feedback limb incorporates the limbic and sensory cortical patterns into a global
activity pattern or order parameter that enslaves all of the components. The
enslavement enhances the coherence among all of them, which dampens the
chaotic fluctuation instead of enhancing it, as the receptor input does in the
sensory cortices.
37 A global operator of this kind must exist, for the following reason. The
synthesis of sense data first into cortical wave packets and then into a
multimodal packet takes time. After a Gestalt has been achieved through
embedding in past experience, a decision is required as to what the organism is
to do next. This also takes time for an evolutionary trajectory through a
sequence of attractors constituting the attractor landscape of possible goals and
actions (Tsuda, 1991). The triggering of a phase transition in the motor system
may occur at any time, if the fluctuations in its multiple inputs are large enough,
thereby terminating the search trajectory. In some emergent behavioral
situations an early response is most effective: action without reflection. In
complex situations with unclear ramifications into the future, precipitate action
may lead to disastrous consequences. More generally, the forebrain appears to
have developed in phylogenetic evolution as an organ taking advantage of the
time provided by distance receptors for the interpretation of raw sense data.
The quenching function of a global operator to delay decision and action can be
seen as a necessary complement on the motor side, to prevent premature
closure of the process of constructing and evaluating possible courses of action.
This view is comparable to that of William James (1879), who wrote: " ... the
study à posteriori of the distribution of consciousness shows it to be exactly
such as we might expect in an organ added for the sake of steering a nervous
system grown too complex to regulate itself.", except that consciousness is not
provided by another "organ" (an add-on part of the human brain) but by a new
hierarchical level of organization of brain dynamics.
38 Action without the deferral that is implicit in awareness can be found in so-
called 'automatic' sequences of action in the performance of familiar complex
routines. Actions 'flow' without awareness. Implicit cognition is continuous, and
it is simply unmasked in the conditions that lead to 'blindsight'. In this view,
emotion is defined as the impetus for action, more specifically, as impending
action. Its degree is proportional to the amplitude of the chaotic fluctuations in
the limbic system, which appears as the modulation depth of the carrier waves
of limbic neural activity patterns. In accordance with the James-Lange theory of
emotion (James 1893), it is experienced through awareness of the activation of
the autonomic nervous system in preparation for and support of overt action, as
described by Cannon (1939). It is observed in the patterns of behavior that
social animals have acquired through evolution (Darwin 1872). Emotion is not
in opposition to reason. Behaviors that are seen as irrational and 'incontinent'
(Davidson 1980) result from premature escape of the chaotic fluctuations from
the leavening and smoothing of the awareness operator. The most intensely
Neurodynamics and Causality 18 Walter J Freeman
emotional behavior, as it is experienced in artistic creation, scientific discovery,
and religious awe, occurs as the intensity of awareness rises in concert with the
strength of the fluctuations (Freeman 1995). As with all other difficult human
endeavors, self-control is achieved through long and arduous practice.
39 Evidence for the existence of the postulated global operator is found in the
high level of covariance in the EEGs simultaneously recorded from the bulb and
the visual, auditory, somatic and limbic (entorhinal) cortices of animals and from
the scalp of humans (Lehmann and Michel 1990). The magnitude of the shared
activity can be measured in limited circumstances by the largest component in
principle components analysis (PCA). Even though the wave forms of the
several sites vary independently and unpredictably, the first component has 50-
70% of the total variance (Smart et al., 1997; Gaál and Freeman, 1997). These
levels are lower than those found within each area of 90-98% (Barrie, Freeman
and Lenhart, 1996), but they are far greater than can be accounted for by any of
a variety of statistical artefacts or sources of correlation such as volume
conduction, pacemaker driving, or contamination by the reference lead in
monopolar recording. The high level of coherence holds for all parts of the
EEG spectrum and for aperiodic as well as near-periodic waves.
40 The maximal coherence appears to have zero phase lag over distances up
to several centimeters between recording sites and even between hemispheres
(Singer and Gray, 1995). Attempts are being made to model the observed zero
time lag among the structures by cancellation of delays in bidirectional
feedback transmission (König and Schillen, 1991; Traub et al. 1996; Roelfsma
et al., 1997).
6. Consciousness viewed as a system parameter controlling chaos
41 A clear choice can be made now between the three meanings of causality
proposed in the Introduction. Awareness and neural activity are not acausal
parallel processes, nor does either make or move the other as an agency in
temporal sequence. Circular causality is a form of explanation that can be
applied at several hierarchical levels without recourse to agency. This
formulation provides the sense or feeling of necessity that is essential for
human comprehension, by addressing the elemental experience of cause and
effect in acts of observation, even though logically it is very different from linear
causality in all aspects of temporal order, spatial contiguity, and invariant
reproducibility. The phrase is a cognitive metaphor. It lacks the attribute of
agency, unless and until the loop is broken into the forward (microsocopic) limb
and the recurrent (macroscopic) limb, in which case the agency that is so
compelling in linear causality can be re-introduced. This move acquiesces to
the needs of the human observers to use it in order to comprehend dynamic
events and processes in the world.
42 I propose that the globally coherent activity, which is an order parameter,
may be an objective correlate of awareness through preafference, comprising
expectation and attention, which are based in prior proprioceptive and
Neurodynamics and Causality 19 Walter J Freeman
exteroceptive feedback of the sensory consequences of previous actions, after
they have undergone limbic integration to form Gestalts, and in the goals that
are emergent in the limbic system. In this view, awareness is basically akin to
the intervening state variable in a homeostatic mechanism, which is both a
physical quantity, a dynamic operator, and the carrier of influence from the past
into the future that supports the relation between a desired set point and an
existing state. The content of the awareness operator may be found in the
spatial pattern of amplitude modulation of the shared wave form component,
which is comparable to the amplitude modulation of the carrier waves in the
primary sensory receiving areas.
43 What is most remarkable about this operator is that it appears to be
antithetical to initiating action. It provides a pervasive neuronal bias that does
not induce phase transitions, but defers them by quenching local fluctuations
(Prigogine, 1980). It alters the attractor landscapes of the lower order
interactive masses of neurons that it enslaves. In the dynamicist view,
intervention by states of awareness in the process of consciousness organizes
the attractor landscape of the motor systems, prior to the instant of its next phase
transition, the moment of choosing in the limbo of indecision, when the global
dynamic brain activity pattern is increasing its complexity and fine-tuning the
guidance of overt action. This state of uncertainty and unreadiness to act may
last a fraction of a second, a minute, a week, or a lifetime. Then when a
contemplated act occurs, awareness follows the onset of the act and does not
precede it.
44 In that hesitancy, between the last act and the next, comes the window of
opportunity, when the breaking of symmetry in the next limbic phase transition
will make apparent what has been chosen. The observer of the self intervenes
by awareness that organizes the attractor landscape, just before the instant of
the next transition:
Between the conception
And the creation
Between the emotion
And the response
Falls the Shadow
Life is very long
T. S. Eliot (1936) The Hollow Men
The causal technology of self-control is familiar to everyone: hold off fear and
anger; defer closure; avoid temptation; take time to study; read and reflect on
the opportunity, meaning, and consequences; take the long view as it has been
inculcated in the educational process. According to Mill (1843): "We cannot,
indeed, directly will to be different from what we are; but neither did those who
are supposed to have formed our characters directly will that we should be what
we are. Their will had no direct power except over their own actions. ... We are
exactly as capable of making our own character, if we will, as others are of
making it for us" (p. 550).
Neurodynamics and Causality 20 Walter J Freeman
45 There are numerous unsolved problems with this hypothesis. Although
strong advances are being made in analyzing the dynamics of the limbic system
and its centerpieces, the entorhinal cortex and hippocampus (Boeijinga and
Lopes da Silva, 1988; O'Keefe and Nadel, 1978; Rolls et al., 1989;
McNaughton, 1993; Wilson and McNaughton, 1993; Buzsaki, 1996;
Eichenbaum, 1997; Traub et al. 1996), their self-organized spatial patterns,
their precise intentional contents and their mechanisms of formation in relation
to intentional action are still unknown. The pyriform cortex to which the bulb
transmits is strongly driven by its input, and it lacks the phase cones that
indicate self-organizing capabilities comparable to those of the sensory
cortices. Whether the hippocampus has those capabilities or is likewise a
driven structure is unknown. The neural mechanisms by which the entire
neocortical neuropil in each hemisphere maintains spatially coherent activity
over a broad spectrum with nearly zero time lag are unknown. The significance
of this coherent activity for behavior is dependent on finding correlates with
behaviors, but these are unknown. If those correlates are meanings, then the
subjects must be asked to make representations of the meanings in order to
communicate them, so that they are far removed from overt behavior.
Knowledge of human brain function is beyond the present reach of
neurodynamics because our brains are too complex, owing to their
mechanisms for language and self-awareness.
7. Causality belongs in technology, not in science
46. The case has now been made on the grounds of neurodynamics that
causality is a form of knowing through intentional action. Thus causality is
inferred not to exist in material objects, but to be assigned to them by humans
with the intent to predict and control them. The determinants of human actions
include not only genetic and environmental factors but self-organizing dynamics
in brains, primarily operating through the dynamics of intentional action, and
secondarily through neural processes that support consciousness, which is
commonly but mistakenly attached to free will. While this inference is not new, it
is given new cogency by recent developments in neuroscience. What, then,
might be the consequences for natural science, philosophy, and medicine, if
this inference is accepted?
47. The concept of causality is fundamental in all aspects of human behavior
and understanding, which includes our efforts in laboratory experiments and the
analysis of data to comprehend the causal relations of world, brain and mind. In
my own work I studied the impact on brain activity of stimuli that animals were
trained to ignore or to respond to, seeking to determine how the stimuli might
cause new patterns of brain activity to form, and how the new patterns might
shape how the animals behaved in response to the stimuli. I attempted to
interpret my findings and those of others in terms of chains of cause and effect,
which I learned to identify as 'linear causality' (Freeman 1975).
48. These attempts repeatedly foundered in the complexities of neural activity
and in the incompatibility of self-organized, goal-directed behavior of my
Neurodynamics and Causality 21 Walter J Freeman
animals with behaviorist models based on input-output determinism. I found
that I was adapting to the animals at least as much as they were being shaped
by me. My resort to acausal correlation based in multivariate statistical
prediction was unsatisfying. Through my readings in physics and philosophy I
learned the concept of 'circular causality', which invokes hierarchical
interactions of immense numbers of semiautonomous elements such as
neurons, which form nonlinear systems.. These exchanges lead to the
formation of macroscopic population dynamics that shapes the patterns of
activity of the contributing individuals. I found this concept to be applicable at
several levels, including the interactions between neurons and neural masses,
between component masses of the forebrain, and between the behaving animal
and its environment, under the rubric of intentionality (Freeman 1995).
49. By adopting this alternative concept I changed my perspective (Freeman
1995). I now sought not to pin events at instants of time, but to conceive of
intervals at differing time scales; not to fill the gaps in the linear chains, but to
construct the feedback pathways from the surround; not to average the single
responses to monotonously repeated stimuli, but to analyze each event in its
uniqueness before generalizing; not to explain events exclusively in terms of
external stimuli and context, but to allow for the contribution of self-organizing
dynamics.
50. Circular causality departs so strongly from the classical tenets of necessity,
invariance, and precise temporal order that the only reason to call it that isto
satisfy the human habitual need for causes The most subtle shift is the
disappearance of agency, which is equivalent to loss of Aristotle's efficient
cause. Agency is a powerful metaphor. For examples, it is common sense to
assert that an assassin causes a victim's death; that an undersea quake causes
a tsunami; that a fallen tree causes a power failure by breaking a transmission
line; that an acid-fast bacillus causes tuberculosis; that an action potential
releases transmitter molecules at a synapse; and so forth. But interactions
across hierarchical levels do not make sense in these terms. Molecules that
cooperate in a hurricane cannot be regarded as the agents that cause the
storm. Neurons cannot be viewed as the agents that make consciousness by
their firing.
51. The very strong appeal of agency to explain events may come from the
subjective experience of cause and effect that develops early in human life,
before the acquisition of language, when as infants we go through the
somatomotor phase (Piaget 1930; Thelen and Smith 1994) and learn to control
our limbs and to focus our sensory receptors. "I act (cause); therefore I feel
(effect)." Granted that causality can be experienced through the neurodynamics
of acquiring knowledge by the use of the body, the question I raise here is
whether brains share this property with other material objects in the world. The
answer I propose is that assignment of cause and effect to one's self and to
others having self-awareness is entirely appropriate, but that investing
insensate objects with causation is comparable to investing them with teleology
and soul.
Neurodynamics and Causality 22 Walter J Freeman
52. The further question is: Does it matter whether or not causality is assigned to
objects? The answer here is: very much. Several examples are given of
scientific errors attributable to thinking in terms of linear causality. The most
important, with wide ramifications, is the assumption of universal determinacy,
by which the causes of human behavior are limited to environmental and
genetic factors, and the causal power of self-determination is excluded from
scientific consideration. We know that linear extrapolation often fails in a
nonlinear world. Proof of the failure of this inference is by reductio ad
absurdum. It is absurd in the name of causal doctrine to deny our capacity as
humans to make choices and decisions regarding our own futures, when we
exercise the causal power that we experience as free will.
8. Anthropocentricity in acts of human observation
53. Our ancestors have a history of interpreting phenomena in human terms
appropriate to the scales and dynamics of our brains and bodies. An example
of our limitations and our cognitive means for surmounting them is our spatial
conception of the earth as flat. This belief is still quite valid for lengths of the
size of the human body, such as pool tables, floors, and playing fields, where
we use levels, transits, and gradometers, and even for distances that we can
cover by walking and swimming. The subtleties of ships that were hull-down
over the horizon were mere curiosities, until feats of intellect and exploration
such as circumnavigation of the earth opened a new spatial scale. Inversely, at
microscopic dimensions of molecules flatness has no meaning. Under an
electron microscope the edge of a razor looks like a mountain range.
54. In respect to time scales, we tend to think of our neurons and brains as
having static anatomies, despite the evidence of continual change from time
lapse cinematography, as well as the cumulative changes that passing decades
reveal to us in our bodies. An intellectual leap is required to understand that
form and function are both dynamic, differing essentially in our time scales of
measurements and experiences with them. The embryological and
phylogenetic developments of brains are described by sequences of geometric
forms and the spatiotemporal operations by which each stage emerges from the
one preceding. The time scales are in days and eons, not in seconds as in
behavior and its neurophysiological correlates.
55. The growth of structure and the formation of the proper internal axonal and
dendritic connections is described by fields of attraction and repulsion, with
gradient descents mediated by contact sensitivities and the diffusion of
chemicals. Moreover, recent research shows that synapses undergo a process
of continual dynamic formation, growth and deletion throughout life (Smythies,
1997). The same and similar terms are used in mathematics and the physical
sciences such as astronomy and cosmology, over a variety of temporal and
spatial scales, many of which are far from the scales of kinesthesia to which we
are accustomed. On the one hand, morphogenesis is the geometry of motion,
which we can grasp intuitively through time lapse photography. On the other
hand, the motions of speeding bullets and hummingbird wings are revealed to
us by high-speed cinematography.
Neurodynamics and Causality 23 Walter J Freeman
56. The attribution of intention as a property of material objects was common in
earlier times by the assignment of spirits to trees, rocks, and the earth. An
example is the rising sun. From the human perspective the sun seems to
ascend above the horizon and move across the sky. In mythology this motion
was assigned to an agency such as a chariot carrying the sun, or to motivation
by the music of Orpheus, because music caused people to dance. In the Middle
Ages the sun, moon, planets and stars were thought to be carried by spheres
that encircled the earth and gave ineffable music as they rotated. The current
geometric explanation is that an observer on the earth's surface shifts across
the terminator with inertial rotation in an acausal space-time relation. Still, we
watch the sun move.
57. Similarly, humans once thought that an object fell because it desired to be
close to the earth, tending to its natural state. In Newtonian mechanics it was
pulled down by gravity. In acausal, relativistic terms, it follows a geodesic to a
minimal energy state. The Newtonian view required action at a distance, which
was thought to be mediated by the postulated quintessence held over from
Aristotle, the "ether". Physicists were misled by this fiction, which stemmed from
the felt need for a medium to transmit a causal agent. The experimental proof
by Michaelson and Morley that the ether did not exist opened the path to
relativistic physics and an implicit renunciation of gravitational causality. But
physicists failed to pursue this revolution to its completion, and instead
persisted in the subject-object distinction by appealing to the dependence of the
objective observation on the subjective reference frame of the observer.
58. In complex, multivariate systems interactive at several levels like brains,
causal sequences are virtually impossible to specify unequivocally. Because it
introduced indeterminacy, evidence for feedback in the nervous system was
deliberately suppressed in the first third of the 20th century. It was thought that
a neuron in a feedback loop could not distinguish its external input from its own
output. An example was the reaction of Ramón y Cajal to a 1929 report by his
student, Rafael Lorente de Nó, who presented Cajal with his Golgi study of
neurons in the entorhinal cortex (Freeman 1984). He constructed diagrams of
axodendritic connections among the neurons with arrows to indicate the
direction of transmission, and he deduced that they formed feedback loops.
Cajal told him that his inference was unacceptable, because brains were
deterministic and could not work if they had feedback. He withdrew his report
from publication until Cajal died in 1934. After he published it (Lorente de Nó
1934), it became an enduring classic, leading to the concept of the nerve cell
assembly by its influence on Donald Hebb (1949), and to neural networks and
digital computers by inspiring Warren McCulloch and through him John von
Neumann (1958). The concept of linear causality similarly slowed recognition
and acceptance of processes of self-organization in complex systems, by the
maxim that "nothing can cause itself." The phrase "self-determination" was
commonly regarded as an oxymoron. A similar exclusion delayed acceptance
of the concept of reafference, also called corollary discharge (Freeman 1995).
9. Applications in philosophy
Neurodynamics and Causality 24 Walter J Freeman
59. Description of a linear causal connection is based on appeal to an invariant
relationship between two events. If an effect follows, the cause is sufficient; if an
effect is always preceded by it, then the cause is necessary. From the temporal
order and its invariance, as attested by double-blind experimental controls to
parcellate the antecedents, an appearance of necessity is derived. The search
concludes with assignment of an agency, that has responsibility for production,
direction, control or stimulation, and that has its own prior agency, since every
cause must also be an effect.
60. According to David Hume (1739), causation does not arise in the events; it
emerges in the minds of the observers. The temporal succession and spatial
contiguity of events that are interpreted as causes and effects comprise the
invariant connection. It is the felt force of conjoined impressions that constitutes
the quale of causality. Since the repetition of these relations adds no new idea,
the feeling of the necessity has to be explained psychologically. He came to
this conclusion from an abstract premiss in the doctrine of the nominalism,
according to which there are no universal essences in reality, so the mind
cannot frame a concept or image that corresponds to any universal or general
term, such as causality. This was opposed, then as now, to the doctrine of
scientific realism. Hume and his nominalist colleagues were anticipated 500
years earlier by the work of Aquinas (1272), who conceived that the individual
forms of matter are abstracted by the imagination ("phantasia") to create
universals that exist only in the intellect, not in matter. Early 20th century
physicists should have completed the Humeian revolution in their development
of quantum mechanics, but they lost their nerve and formulated instead the
Copenhagen interpretations, which reaffirmed the subject-object distinction of
Plato and Descartes, despite the force of their own discoveries staring them in
the face. Phenomenologists before Heidegger maintained the error, and
postmodern structuralists persist in it. For example, instead of saying,
"Causality is a form of knowing", they say, "The attribution of causality is a form
of knowing." That is, "Causality really does exist in matter, but it is a matter of
choice by humans whether to believe it."
61. Conversely, John Stuart Mill (1873) accepted "the universal law of
causation" but not necessity. "... the doctrine of what is called Philosophical
Necessity" weighed on my existence like an incubus. ... I pondered painfully on
the subject, till gradually I saw light through it. I perceived, that the word
Necessity, as a name for the doctrine of Cause and Effect applied to human
action, carried with it a misleading association; and that this association was the
operative force in the depressing and paralyzing influence which I had
experienced" (pp. 101-102). He developed his position fully in "A System of
Logic" (1843).
62. Kant (1781) insisted that science could not exist without causality. Since
causality was for him a category in mind, it follows that science is a body of
knowledge about the world but is not in the world. Causality then becomes a
basis for agreement among scientists regarding the validation of relationships
between events, and the prediction of actions to be taken for control of events in
Neurodynamics and Causality 25 Walter J Freeman
the world. Since it could not be validated by inductive generalization from
sense data, but was nevertheless essential to give wholeness and completion
to experience [Apperzeption], Kant concluded that it must be "a priori" and
"transcendental" over the sense data. This led him to designate causality as a
category [Kategorien] in and of the mind, along with space and time as the
forms of perception [Anschauungsformen], by which the sense data were
irretrievably modified during assembly into perceptions, making the real world
[Ding an sich] inaccessible to direct observation.
63. Friedrich Nietzsche (1886) placed causality in the mind as the expression of
free will: "The question is in the end whether we really recognize the will as
efficient, whether we believe in the causality of the will: if we do -- and at bottom
our faith in this is nothing less than our faith in causality itself -- then we have to
make the experiment of positing the causality of the will hypothetically as the
only one ... the will to power" (p. 48).
64. Putnam (1990) assigned causality to the operation of brains in the process
of observation: "Hume's account of causation ... is anathema to most present-
day philosophers. Nothing could be more contrary to the spirit of recent
philosophical writing than the idea that there is nothing more to causality than
regularity or the idea that, if there is something more, that something more is
largely subjective." (p. 81) "If we cannot give a single example of an ordinary
observation report which does not, directly or indirectly, presuppose causal
judgments, then the empirical distinction between the "regularities" we
"observe" and the "causality" we "project onto" the objects and events involved
in the regularities collapses. Perhaps the notion of causality is so primitive that
the very notion of observation presupposes it?" [p. 75]
65. A case was made by Davidson (1980) for "anomalous monism" to resolve
the apparent contradiction between the deterministic laws of physics, the
necessity for embodiment of mental processes in materials governed by those
fixed laws, and the weakness of the "laws" governing psychophysical events as
distinct from statistical classes of events: "Why on earth should a cause turn an
action into a mere happening and a person into a helpless victim? Is it because
we tend to assume, at least in the arena of action, that a cause demands a
causer, agency and agent? So we press the question; if my action is caused,
what caused it? If I did, then there is the absurdity of an infinite regress; if I did
not, I am a victim. But of course the alternatives are not exhaustive. Some
causes have no agents. Among these agentless causes are the states and
changes of state in persons which, because they are reasons as well as
causes, constitute certain events free and intentional actions." [p. 19]
66. His premisses have been superceded in two respects. First, he postulated
that brains are material systems, for which the laws of physics support accurate
prediction. He described brains as "closed systems". In the past three decades
numerous investigators have realized that brains are open systems, as are all
organs and living systems, with an infinite sink in the venous return for waste
heat and entropy, so that the 1st and 2nd laws of thermodynamics do not hold
for brains, thus negating one of his two main premisses. Second, he postulated
Neurodynamics and Causality 26 Walter J Freeman
that, with respect to meaning, minds are "open" systems, on the basis that they
are continually acting into the world and learning about it. The analyses of
electrophysiological data taken during the operations of sensory cortices during
acts of perception indicate that meaning in each mind is a closed system, and
that meaning is based in chaotic constructions, not in information processing,
thus negating the other of his two main premisses. In my view, neurons engage
in complex biochemical operations that have no meaning or information in
themselves, but inspire meaning in researchers who measure them. The
degree of unpredictability of mental and behavioral events is in full accord with
the extent of variations in the space-time patterns of the activity of chaotic
systems, thus removing the requirement for the adjective, "anomalous",
because it applies to both sets of laws for the material and mental aspects of
living systems. Moreover, the adoption of the concept "circular causality" from
physics and psychology removes agency. That which remains is "dynamical
monism".
10. Applications of causality in medical technology
67. Causality is properly attributed to intentional systems, whose mechanisms of
exploring, learning, choosing, deciding, and acting constitute the actualization
of the feeling of necessary connection, and of the cognitive metaphor of agency.
It is properly used to describe technological intervention into processes of the
material world after analysis of the interrelations of events. Surmounting linear
causal thinking may enable neuroscientists to pursue studies in the dynamics of
the limbic system to clarify the meanings of statistical regularities in chaotic, self-
organizing systems and change their outcomes by experimental manipulation.
Social scientists may take advantage of the discovery of a biological basis for
choice and individual responsibility to strengthen our social and legal
institutions by complementing environmental and genetic linear causation. The
nature-nurture debate has neglected a third of the determinant triad: the self
People can and do make something of themselves. Neurophilosophers
studying consciousness in brain function may find new answers to old
questions by re-opening the debate on causality. What acausal relations arise
among the still inadequately defined entities comprising brains? What is the
global operator of consciousness? The mind-brain problem is not solved, but it
can be transplanted to more fertile ground.
68. My proposal is not to deny or abandon causality, but to adapt it as an
essential aspect of the human mind/brain by virtue of its attachment to
intentionality. This can be done by using the term "circular causality" divorced
from agency in the sciences, and the term "linear causality" in combination with
agency in the technologies, including medical, social, legal, and engineering
applications.
69. For example, medical research is widely conceived as the search for the
causes of diseases and the means for intervention to prevent or cure them. A
keystone in microbiology is expressed in Koch's Postulates, which were
formulated in 1881 by Robert Koch to specify the conditions that must be met, in
order to assign a causal relation between a microorganism and a disease:
Neurodynamics and Causality 27 Walter J Freeman
(1) the germ must always be found in the disease; (2) it must be isolated
in pure culture from the diseased individual; (3) inoculation with the
isolated culture must be followed by the same disease in a suitable test
animal; and (4) the same germ must be isolated in pure culture from the
diseased test animal.
70. These postulates have served well for understanding transmissible
diseases and providing a biological foundation for developing chemotherapies,
vaccines, and other preventatives. Public health measures addressing
housing, nutrition, waste disposal and water supplies had already been well
advanced in the 19th century for the prevention of pandemics such as cholera,
typhoid, tuberculosis, and dysentery, on the basis of associations and to a
considerable extent the maxim, "Cleanliness is next to Godliness". This was
intentional behavior of a high order indeed. The new science brought an
unequivocal set of targets for research on methods of prevention and treatment.
71. The most dramatic development in neuropsychiatry was the finding of
spirochetes in the brains of patients with general paresis, for which the
assigned causes had been life styles of dissolution and moral turpitude. The
discovery of the "magic bullet" 606 (arsphenamine) established the medical
model for management of neuropsychiatric illness, which was rapidly extended
to viruses (rabies, polio, measles), environmental toxins (lead, mercury, ergot),
vitamin and mineral deficiencies (cretinism, pellagra), hormonal deficits
(hypothyroidism, diabetic coma, lack of dopamine in postencephalitic and other
types of Parkinson's disease), and genetic abnormalities (phenylketonuria,
Tourette's and Huntingdon's chorea). Massive research programs are under
way to find the unitary causes and the magic bullets of chemotherapies,
replacement genes, and vaccines for Alzheimer's, neuroses, psychoses, and
schizophrenias. The current explanations of the affective disorders -- too much
or too little dopamine, serotonin, etc. -- resemble the Hippocratic doctrine of the
four humors, imbalances of which were seen as the causes of diseases.
72. There are compelling examples of necessary connections. Who can doubt
that the vibrio causes cholera, or that a now eradicated virus caused small pox?
However, these examples come from medical technology, in which several
specific conditions hold. First, the discoveries in bacteriology came through an
extension of human perception through the microscope to a new spatial scale.
This led to the development by Rudolf Virchow of the cellular basis of human
pathology. The bacterial adversaries were then seen as having the same
spatial dimensions as the cells with which they were at war. The bacterial
invaders and the varieties of their modes of attack did not qualitatively differ
from the macroscopic predators with which mankind had always been familiar,
such as wolves and crocodiles, which humans eradicate, avoid, or maintain in
laboratories and zoos. Second, the causal metaphor motivated the application
of controlled experiments to the isolation and analysis of target bacterial and
viral species, vitamins, toxic chemicals, hormones, and genes. It still does
motivate researchers, with the peculiar potency of intermittent reinforcement by
occasional success. The latest example is the recognition that pyloric ulcers
Neurodynamics and Causality 28 Walter J Freeman
are caused by a bacillus and not by psychic stress or a deleterious life style,
implying that the cause is "real" and not just "psychosomatic". Third, the
research and therapies are directly addressed to humans, who take action by
ingesting drugs and seeking vaccinations, and who perceive changes in their
bodies thereafter. A feeling of causal efficacy is very powerful in these
circumstances, and many patients commit themselves without reservation to
treatments, well after FDA scientists by controlled studies have shown them to
be ineffective. The urgency of conceptualizing causality to motivate beneficial
human actions does not thereby establish the validity of that agency among the
objects under study. Feeling is believing, but it is not knowing. The feeling of
causal agency in medicine has led to victories, but also to mistakes with injury
and death on a grand scale.
73. Koch's postulates approach a necessary connection of a bacillus to an
infectious disease, but not the sufficient conditions. Pathogens are found in
healthy individuals as well, and often not in the sick. Inoculation does not
always succeed in producing the disease. These anomalies can be, and
commonly are, ignored, if the preponderance of evidence justifies doing so, but
the classical criteria for causality are violated, or are replaced with statistical
judgments. A positive culture of a bacillus is sufficient reason to initiate
treatment with an antibiotic, even if it is the wrong disease. Similarly,
pathologists cannot tell the cause of death from their findings at autopsy. They
are trained to state what the patient died "with" and not "of". It is the job of the
coroner or a licensed physician to assign the cause of death. The causes of
death are not scientific. They are social and technological, and they concern
public health, economic well being, and the apprehension of criminals.
74. Another example of the social value of causality is the statement: "Smoking
causes cancer." This is a clear and valid warning that a particular form of
behavior is likely to end in early and painful death. On the one hand, society
has a legitimate interest in maintaining health and reducing monetary and
emotional costs by investing the strong statistical connection with the motivating
status of causality. On the other hand, the "causal chain" by which tobacco tars
are connected to the unbridled proliferation of pulmonary epithelial tissue is still
being explored, and a continuing weakness of evidence for the complete linear
causal chain is being used by tobacco companies to claim that there is no proof
that smoking causes cancer. Thus the causal argument has been turned
against society's justifiable efforts to prevent tobacco-related illnesses.
11. The Technology of Mental Illness
76. The most complex and ambiguous field of medicine concerns the causes
and treatments of mental disorders. Diagnosis and treatment for the past
century have been polarized between the medical model of the causes of
diseases, currently held in biological psychiatry, and psychoanalysis, the talking
cure. Sigmund Freud was impressed with the phenomena of hysteria, in which
patients suffered transient disabilities, such as blindness and paralysis, but
presented no evidence of infection or anatomical degeneration in their brains.
He drew on his background in clinical neurology to develop a biological
Neurodynamics and Causality 29 Walter J Freeman
hypothesis (1895) for behavior, based on the flow of nerve energy between
neurons through "contact barriers" (3 years later named synapses by Foster and
Sherrington). Some axonal pathways developed excessive resistance at these
barriers, deflecting nerve energy into unusual channels by "neuronic inertia",
giving rise to hysterical symptoms. Within a decade he had abandoned the
biological approach as "premature", working instead with his symbolic model of
the id, ego, and superego, but his ideas were generalized to distinguish
"functional" from "organic" diseases. Traumatic childhood experiences warped
the development of the contact barriers. Treatment was to explore the recesses
of memory, bring the resistances to awareness, and reduce them by client and
therapist reasoning together following transference and countertransference.
77. The bipolarization between the organic and the functional has been stable
for a century. Patients and practitioners have been able to choose their
positions in this spectrum of causes according to their beliefs and preferences.
Some patients are delighted to be informed that their disorders are due to
chemical imbalances, that are correctable by drugs and are not their fault or
responsibility. Others bitterly resent the perceived betrayal by their bodies, and
they seek healing through the exercise of mental discipline and the power of
positive thinking. But the balance has become unstable with two new
circumstances. One is the cost of medical care. Health maintenance
organizations are pressuring psychiatrists to see more patients in shorter visits,
to dispense with oral histories and the meanings of symptoms for the patients,
and to get them quickly out the door with packets of pills. The power of
biological causality is clearly in operation as a social, not a scientific, impetus,
operating to the detriment of people with complex histories and concerns.
78. The other circumstance is the growing realization among mental health care
specialists that chemical imbalances, poor genes, and unfortunate experiences
of individuals are insufficient explanations to provide the foundations for
treatment. Of particular importance for onset, course, and resolution of illnesses
are the social relations of individuals, their families, neighborhoods, religious
communities, and milieu of national policies and events. Current conflicts rage
over the assignment of the cause of chronic fatigue syndrome to neuroticism or
to a virus; of the Gulf War syndrome to malingering or a neurotoxin; of post-
traumatic stress disorder to battle fatigue or a character deficit. The
dependence of the debates on causality is fueled by technological questions of
human action: what research is to be done, what treatments are to be given,
and who is to pay for them? Successful outcomes are known to depend less on
pills and counseling than on mobilization of community support for distressed
individuals (Frankl, 1973). These exceedingly complex relations, involving faith
and meaning among family and friends, may be seriously violated by reduction
to unidirectional causes. Patients may be restored to perfect chemical balance
and then die anyway in despair. Families may disintegrate into endless
recrimination and self-justification, from lack of tolerance of misdirected parental
and filial intentions and honest mistakes. So it is with patient-doctor relations.
To seek and find a cause is to lay the blame, opening the legal right to sue for
compensation for psychological injury and distress. These, too, are legacies of
linear causal thinking.
Neurodynamics and Causality 30 Walter J Freeman
79. Abnormal behavior in states of trance or seizure was attributed in past
centuries to the loss or willing surrender of self-control to possession by exotic
spirits. In the West the failure of responsibility was codified as legal insanity in
1846 according to the McNaughton Rule: "[To] establish a defense on the
grounds of insanity, it must be clearly proven that at the time of the committing of
the act, the party accused was labouring under such a defect of reason, from
disease of the mind, as not to know the nature and quality of the act he was
doing, or, if he did know it, that he did not know he was doing what was wrong."
In the terms of the present analysis, for behavior to be insane the neural
components of the limbic system must have entered into basins of attraction that
are sufficiently strange or unusually stable to escape control by the global state
variable. This view encompasses the two facets of causality, microscopic and
macroscopic, that compete for control of the self, but it is not an adequate
statement of the problem. In fact the case on which the Rule was based was
decided on political grounds (Moran 1981). Daniel McNaughton was a
Scotsman engaged in ideal-driven assassination, and his transfer by the British
authorities from Newgate Prison to Bethlam Hospital was designed to prevent
him from testifying in public. A similar move for similar reasons was made by
the American government by sending the poet Ezra Pound, charged with
treason in World War II, to St. Elizabeth's Hospital instead of the Leavenworth.
The point is that judgments about which acts are intentional and which are not
are made by society, in last resort by judges and juries in courts of law, not by
doctors, scientists, or individuals in isolation. What biology can offer is a
foundation on which to construct a social theory of self-control.
12. The science versus the technology of self-control
80. The role of causality in self-awareness is close to the essence of what it is
to be human. Nowhere is this more poignant than in the feeling of the need for
self-control. Materialists and psychoanalysts see the limbic self as a machine
driven by metabolic needs and inherited instincts, the id, that carries the ego as
a rational critic that struggles to maintain causal control, as befits the Cartesian
metaphor of the soul serving as the pilot of a boat, by adjudicating blind forces.
Structure and chemistry are genetically determined. Behaviorist psychologists
confuse motivation with intention and view behavior as the sum of reflexes,
caused by environmental inputs and sociobiological processes, while
consciousness is epiphenomenal.
81. Functionalists see the mind as equivalent to software that can be adapted to
run on any platform, once the algorithms and rules have been discovered.
Logical operations on symbols as representations are the causes of rational
behavior, and the unsolved problems for research concern the linkage of the
symbols with activities of neurons and with whatever the symbols represent in
the world. That research will be unnecessary, if the linkages can made instead
to the components of intelligent machines resembling computers (Fodor 1981).
Unfortunately the only existing intelligent beings have evolved from lower
species, and our brains contain the limbic system as irrational baggage.
Outputs from the logic circuits in the neocortex, before reaching the motor
Neurodynamics and Causality 31 Walter J Freeman
apparatus, are filtered through the limbic system, where emotions are attached
that distort and degrade the rational output. Consciousness is a mystery to be
explained by 'new laws of physics' (Penrose 1994; Chalmers 1996).
82. Existentialists hold that humans choose what they become by their own
actions. The cause of behavior is the self, which is here described as emerging
through the dynamics in the limbic system. The ego constituting awareness of
the self discovers its own nature by observing and analyzing its actions and
creations, but cannot claim credit for them. In extreme claims advanced by
Nietzsche and Sartre the ego is unconstrained by reality. In more modest
terms, because of the circularity of the relation of the self and its awareness, the
future actions of the self are shaped in the context of its irrevocable past, its
body, its given cultural and physical environment, and its present state of
awareness, which is its own creation. The finite brain grapples with the infinity
of the world and the uncertainty of the interlocked futures of world and brain, by
continually seeking the invariances that will support reliable predictions. Those
predictions exist as awareness of future possibilities, without which the self
cannot prevail. They are expressed in the feeling of hope: the future need not
merely happen; to some extent it can be caused.
13. Conclusion
83 The interactions between microscopic and macroscopic domains lie at the
heart of self-organization. How do all those neurons simultaneously get
together in a virtual instant, and switch from one harmonious pattern to another
in an orderly dance, like the shuttle of lights on the "magic loom" of Sherrington
(1940)? The same problem holds for the excitation of atoms in a laser, leading
to the emergence of coherent light from the organization of the whole mass; for
the coordinated motions of molecules of water and air in a hurricane; for the
orchestration of the organelles of caterpillars in metamorphosing to butterflies;
and for the inflammatory spread of behavioral fads, rebellions, and revolutions
that sweep entire nations. All these kinds of events call for new laws such as
those developed in physics by Haken (1983), in chemistry by Prigogine (1980),
in biology by Eigen and Schuster (1979), in sociology by Foucault (1976), and
in neurobiology by Edelman (1987), which can address new levels of
complexity that have heretofore been inaccessible to human comprehension.
Perhaps these will serve as the "new laws" called for by Penrose (1994) and
Chalmers (1996), but they need not lead to dualism or panpsychism. They can
arise as logical extensions from the bases of understanding we already have in
these several realms of science, none of which can be fully reduced to the
others.
84. Consciousness in the neurodynamic view is a global internal state variable
composed of a sequence of momentary states of awareness. Its regulatory role
is comparable to that of the operator in a thermostat, that instantiates the
difference between the sensed temperature and a set point, and that initiates
corrective action by turning a heater on or off. The machine state variable has
little history and no capacities for learning or determining its own set point, but
the principle is the same: the internal state is a form of energy, an operator, a
Neurodynamics and Causality 32 Walter J Freeman
predictor of the future, and a carrier of information that is available to the system
as a whole. It is a prototype, an evolutionary precursor, not to be confused with
awareness, any more than tropism in plants and bacteria is to be confused with
intentionality. In humans, the operations and informational contents of the
global state variable, which are sensations, images, feelings, thoughts and
beliefs, constitute the experience of causation.
85. To deny this comparability and assert that humans are not machines is to
miss the point. Two things distinguish humans from all other beings. One is the
form and function of the human body, including the brain, which has been given
to us by three billion years of biological evolution. The other is the heritage
given to us by two million years of cultural evolution. Our mental attributes have
been characterized for millennia as the soul or spirit or consciousness that
makes us not-machines. The uniqueness of the human condition is not thereby
explained, but the concept of circular causality provides a tool for intervention,
when something has gone wrong, because the circle can be broken into
forward and feedback limbs. Each of them can be explained by linear causality,
which tells us where and how to intervene. The only error would be to assign
causal agency to the parts of the machine.
14. Summary
86. Science provides knowledge of relations among objects in the world,
whereas technology provides tools for intervention into the relations by humans
with intent to control the objects. The acausal science of understanding the self
distinctively differs from the causal technology of self-control. "Circular
causality" in self-organizing systems is a concept that is useful to describe
interactions between microscopic neurons in assemblies and the macroscopic
emergent state variable that organizes them. In this review intentional action is
ascribed to the activities of the subsystems. Awareness (fleeting frames) and
consciousness (continual operator) are ascribed to a hemisphere-wide order
parameter constituting a global brain state. Linear causal inference is
appropriate and essential for planning and interpreting human actions and
personal relations, but it can be misleading when it is applied to microscopic-
microscopic relations in brains. It is paradoxical to assign linear causality to
brains, and thereby cast doubt on the validity of causal agency (free will) in
choices in and by humans, just because they are materialized in phase
transitions in their brains.
Acknowledgements
This research was supported by grants from the National Institutes of Health
MH-06686 and the Office of Naval Research N00014-93-1-0938
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