The Competitiveness of Nations in a Global Knowledge-Based Economy
Walter J Freeman
Emotion is Essential to All Intentional
Behaviors
Chapter 8 in:
Emotion, Development, and
Self-Organization Dynamic Systems Approaches to Emotional
Development
Marc D. Lewis & Isabel Granic (Eds).
Walter J Freeman
Department of Molecular & Cell
Biology
wfreeman@socrates.berkeley.edu
tel 510-642-4220 fax
510-643-6791
http://sulcus.berkeley.edu/wjf/CE.%20Neurodynamics.and.Emotion.pdf
page 1
Emotion is defined as a property of intentional
behavior. The widespread practice
of separating emotion from reason is traced to an ancient distinction between
passive perception, which is driven by sensory information from the environment,
and active perception, which begins with dynamics in the brain that moves the
body into the environment in search of stimuli. The neurodynamics of intentional behavior
is reviewed, with emphasis on the limbic system that controls the autonomic and
neuroendocrine systems in the brain and body, directing them for the support of
the musculoskeletal system that is executing the behavior. An essential part of intentionality is
learning from the sensory consequences of one's own actions. The perception of emotional states
through awareness involves global states of cooperative activity in the
forebrain, which have internal contributions from the many parts of the brain
that join in making these states, and inevitably there are contributions from
the sensory systems of the body that implement and signal emotional states. The distinction between "rational"
versus "emotional" behaviors is made in terms of the constraint of
high-intensity chaotic activity of components of the forebrain by the
cooperative dynamics of consciousness versus the escape of subsystems owing to
an excess of chaotic fluctuations in states of strong
arousal.
1
The problem of understanding emotion has emerged as one
of the major challenges for the social, psychological, and psychiatric
disciplines. The root of the
problem goes very deeply into the history of Western science and philosophy,
whence came the primary assumptions that people of European origin use to
explain the nature of mind, and how the mind relates to the body and to the
world through learning. A singular
clue to the form of one of these assumptions is provided by the distinction
often made between emotion and reason. This is a "common sense" notion used to
explain the motives of observed behaviors. Motives are reasons that explain the
actions we witness with respect to the state of mind of the perpetrators. In this philosophical interpretation,
actions stem either from reasoned judgments of available options in the light of
self interest or the greater good, or they are based in an internal force that
is out of conscious control and beyond rational choice - blind
emotion.
An alternative view, one that I will elaborate here,
holds that because this dichotomy treats emotion as bad and reason as good, it
fails to recognize them as properties of a larger whole. All actions are emotional, and at the
same time they have their reasons and explanations. This is the nature of intentional
behavior. I will begin with a
historical review of the philosophical grounds in which this dichotomy arose and
will follow that review with a description of brain function in the genesis of
intention through the nonlinear dynamics of neural populations. I will conclude with some remarks on the
interrelation of consciousness and emotion, in an attempt to recast the
distinction between rational and emotional people in the light of
neurodynamics.
A major cleavage that fuels debates on the nature of
mind derives the ancient Greeks: Is perception active or passive? According to Plato it was passive. He drew a distinction between intellect
and sense, both being immaterial and belonging to the soul. The intellect was born with ideal forms
of objects in the world, and the senses presented imperfect copies of those
forms. For each object the
intellect sought the corresponding subjective ideal form through the exercise of
reason. Thus the experiences from
the world of objects and events were passively impressed onto the senses. According to Aristotle it was active.
There were no ideal forms in the
mind. The organism moved in
accordance with its biological destiny, which was initiated by the Prime Mover
(God). The actions of the intellect
were to define and seek objects with its sensorimotor power, and with its
cogitative power to construct forms of them by abstraction and induction from
the examples that were presented by the senses. The forms of mental contents from stimuli
were inscribed by the intellect with its mnemonic power onto an initially blank
slate, the "tabula rasa". Emotion
was treated in both systems as an aspect of the animality of man, the rational
animal, which was a residue of corporeality that was to be subjugated by
reason.
In the early Middle Ages the Platonic view was dominant through the work of
Q12 Of Intention
"A1: Whether intention is an act of the intellect or of
the will? Intention, as the very
word denotes, means to tend to something. Now both the action of the mover and the
movement of the thing moved tend to something. But that the movement of the thing moved
tends to anything is due to the action of the mover. Consequently intention belongs first and
principally to that which moves to the end; hence we say that an architect or
anyone who is
2
in authority, by his command moves others to that which
he intends. Now the will moves all
the other powers of the soul to the end. Therefore it is evident that intention,
properly speaking, is an act of the will ... in regard to the end. Now the will stands in a threefold
relation to the end. First,
absolutely. And in this way we have
volition, whereby we will absolutely to have health and so forth. Secondly, it considers the end, as its
place of rest. And in this way
enjoyment regards the end. Thirdly,
it considers the end as the term towards which something is ordered; and thus
intention regards the end. For when
we speak of intending to have health, we mean not only that we will to have it,
but that we will to have it by means of something else."
"A4: Whether intention of the end is the same act as the
volition of the means? Accordingly,
in so far as the movement of the will is to the means, as ordered to the end, it
is called choice; but the movement of the will to the end as acquired by the
means, is called intention. A sign
of this is that we can have intention of the end without having determined the
means which are the object of choice."
This distinction between will or volition based in
choice (for which we might now read "consciousness") and intent (which may or
may not be conscious) was rapidly and wholeheartedly adopted by the Western
European community, and it had far-reaching consequences for the growth of
middle class morality and the belief in the capability of individuals to accept
responsibility and take action to change things in the world that needed
changing. In my opinion the growth
of science and technology through the later Middle Ages in large part stemmed
from that liberation and its philosophical justification of individual freedom.
However, emotions were not given
the status assigned to will nor clearly distinguished from intent. Consciousness is a modern concept for
which no real equivalent exists in ancient or medieval world views, and emotions
appear to be best translated as the "passions" of the soul, in reference to
suffering from external forces foreign to one's true
nature.
During the Renaissance Western thought returned to Plato
largely through the work of Descartes, who conceived a revolutionary approach of
describing the world and the mind in terms of linear algebra and geometry,
without place for the faculty of imagination. In his view the animal machine in man was
guided by the soul as its "pilot", who sought knowledge through reasoning about
the passive imprints of sensations, in order to come to absolute mathematical
truth. Fantasy, intention, and
emotion were dismissed along with imagination as being non mathematical and
therefore unscientific. The origin
of "passions" coming from outside one's true nature was left
unexplained.
In the postmodern era Descartes' pilot has been fired.
The reasons usually given are
either that the soul does not exist, or that the concept doesn't explain
anything, or that the soul is a matter of personal belief, not a scientific
principle. In philosophy
intentionality was reinstated in modified form by Franz Brentano (1889) to
signify the relations between representations in the mind and objects in the
world, and thereby to distinguish humans from machines. In the medical and biological sciences,
explanations of the mind are sought in terms of the functions of the body
through studies in behavior, and by analysis of the brain through chemistry and
imaging. Emotions have become
matters of central concern, particularly in the context of the affective
disorders, where the tendency has been to see them as determined by the
machinery of the brain, and most recently by the family of neurohormones in the
brain stem, but not in relation to volition or intention.
There is another and less easily grasped reason for the decline of confidence in the Cartesian pilot. For the past three centuries the functions of mind and brain have been described in terms of the linear dynamics of
3
of objects and events from the environment, which is
called information processing. Mental contents are seen as formed by
neural connections that are determined by genes, and modified by learning from
stimuli, particularly during critical periods of growth. Representations of objects and events are
stored in memory banks as ideal forms, each having attached to it a label as to
its value for the organism, and they are used to classify new inputs by
retrieval, cross-correlation, template matching, error reduction, modification
of wiring in neural networks by Hebbian synapses, and assignment of value by
passage through the emotional generators of the brain in the basal ganglia and
brain stem. Questions of how the
brain can a priori create its own goals and then find the appropriate
search images in its memory banks are not well handled. The loss of the Cartesian pilot has left
a large gap in the theory, because no one wants a homunculus, but cognitivists
have no replacement.
In the first half of the 20th century some pragmatists,
existentialists and Gestaltists broke from the Platonic tradition by
incorporating concepts of the source of value in action (Dewey, 1914), the
importance of pre-existing goals and expectations (Merleau-Ponty, 1945), and the
role of affordances in governing perceptions (Gibson, 1979). Merleau-Ponty drew heavily on the
clinical neurology of his epoch to reintroduce intentionality in its Thomist
sense, as the outward "tending" of brain activity with sensory consequences that
completed what he called the "intentional arc". Despite the strong neural basis of these
concepts, most neuroscientists have failed to respond to or accommodate them, in
part because of their complexity, but in larger part because of the lack of a
coherent theory of the deep origin of goal-structures in brains of animals and
humans.
However, in the second half of this century a sharp
break in the mathematical, physical and chemical sciences has occurred with the
development of nonlinear dynamics, which was made possible by the emergence of
computer technology. Recognition of
"dissipative structures" by Prigogine (1980), of "macroscopic order parameters"
by Haken (1983), and of "positive entropic information flows" by various authors
writing on self-organization in chaotic systems has opened new avenues to pursue
the age-old question: "How do goals and their derivative values and expectancies
arise in brains?" Proposed new
answers are expressed in terms of "circular causality" in philosophy
(Cartwright, 1989), psychology (Rosch, 1994) and physics (Haken, 1983), which is
a convenient term to address the intrinsic indeterminacy of feedback, by which
the components of a system can in large part determine their own behavior. The theory of chaos and nonlinear
dynamics, when applied to the functions of brains, can answer the fundamental
mystery faced by the concept of intent, by showing how goals, their attendant
values, and the creative actions by which they are pursued can arise in brains.
Every intentional act is preceded
by the formation of its character prior to its execution. And if perception is active, then things
that are perceived in the body and the world must in an important sense
pre-exist in the sensory cortices as the predicted consequences of acts of
searching.
Emotion as the anticipation of intentional
action
Intentional action begins with the emergent construction
within the brain of goals comprising its possible future states, which will
require that actions be directed by the brain in order that those futures be
realized. The departure from a
state of calm rest without anticipation is aptly named: e(x)motion ("ex" =
"outward"). An emotional state need
not be revealed in immediate overt actions, but it certainly implies the high
probability of actions that will soon be directed outward from an individual
into the world. Such states are
easily recognized and explained as intentional in many situations, but in others
they seem to boil up spontaneously and illogically within an individual in
defiance of intent. The behaviors
may be in apparent contradiction to sensory triggers that seem trivial,
contrary, or insufficient to account for the intensity of actions. Yet they may have an internal logic that
comes to light only after probing into and reflecting on the history of the
individual. Philosophers refer to
such actions as "incontinent" (Davidson, 1980).
A way of making sense of emotion is to identify it with
the intention to act in the near future, and then to note increasing levels of
the complexity of contextualization. Most basically, emotion
is
4
outward movement. It is the "stretching forth" of
intentionality, which is seen in primitive animals preparing to attack in order
to gain food, territory, resources to reproduce, or to find shelter and escape
impending harm (Panksepp, 1998). The key characteristic is that the action
wells up from within the organism. It is not a reflex. It is directed toward some future state,
which is being determined by the organism in conjunction with its perceptions of
its evolving condition and its history. This primitive form of emotion is called
"motivation" or "drive" by behaviorists. These are bad choices of terms, because
they confuse intention, which is action that is to be taken, with biological
imperatives such as the need for food and water, which are the reasons and
explanations for the actions. Behaviorists (passivists) treat behaviors
as fixed action patterns released by stimuli from the environment, and they
cannot explain phenomena such as curiosity, self-improvement, and
self-sacrifice. Their terms are
also commonly conflated with arousal, which is a nonspecific increase in the
sensitivity of the nervous system, that need not be locked into any incipient
action. In other words, the
concepts of motivation and drive lack the two key properties of emotion, which
are endogenous origin and intentionality, and I propose to avoid using
them.
At a more physiological level, emotion includes the
behavioral expression of internal states of the brain. The behaviors that are directed through
interactions with the world toward the future state of an organism predictably
require adaptations of the body to support the intentional motor activity. These preparations consist of taking an
appropriate postural stance with the musculoskeletal system, and mobilizing the
metabolic support systems. The
latter include the cardiovascular, respiratory, and endocrine systems, that will
be called upon to supply oxygen and nutrients to the muscles, to remove the
waste products of energy expenditure, and to facilitate oxidative catabolism.
It is the directedness of these
preparations in the positioning of the body, the heightening of respiration, the
twitching of the tail, and so on, that reveal to observers the emergence of the
likelihood of approach, attack or escape.
Among social animals that live in packs and tribes, these preparatory changes in the body of an organism have become, through evolutionary adaptation, external representations of internal states of meaning and expected action. The display of panting, pawing, stomping the ground, erecting the hair or sexual organs, or moving the face or limbs can serve as signals from each organism to others in its surround (
At a more complex level, emotions are experiences. They are the feelings that accompany the
emergent actions that address the anticipated futures of gain or loss in one's
attachments to others, one's livelihood and safety, and the perceived
possibility or impossibility of changing the world to one's liking or advantage:
joy, grief, fear, rage, hope and despair. Though we associate them with objects in
the world, these feelings, which philosophers call qualia, are internally
derived and do not belong to those objects, such as the sweetness of fruit, the
repugnance of carrion, the inviting softness of velvet, and so
on.
The mechanisms of these feelings remain in dispute.
The physiologist Walter Cannon, in
the passivist-materialist tradition, identified them with the activity of
neurons in the head ganglion of the autonomic nervous system, which is in the
hypothalamus. The psychologist
William James (1890), in the activist-pragmatist tradition, proposed that the
feelings were sensed after the fact, so to speak, through the changes in the
body that were made by the activity of the autonomic nervous system, such as the
sinking of the stomach, which is known to occur in states of fear, the bristling
of hairs in the skin, the pounding of the pulse, the flushing of the face, and
so on. Physiologists view these
feelings as epiphenomena. Pragmatists see them as integral parts of
the ongoing interaction between one's self and one's social environment. Through these bodily processes one
becomes aware of one's emotional state, and, through those signals, one's
friends can typically become aware of that state at the same time as one's self.
The perception of one's own action
and state, and of the states and actions of one's friends, shapes the basis for
one's own next action. It
5
is neither necessary nor feasible to separate the
expression of autonomic states and one's perceptions of them in the intentional
loop. They evolve as an organic
whole.
The perception of feelings requires the process of
awareness. Behavior without
awareness is called automatic, instinctive, unthinking, and implicitly
cognitive. Acting in accustomed
roles, engaging in highly practiced sports routine, and driving a car are
examples. Are they emotional? Competitive sports and dramatic
performances are obviously so. Evidence that driving a car is intensely
emotional is found in the frenzy of concern that a fuel shortage causes, and in
the lavish care that many owners give their machines, even in priority over
their families. A behavioral action
cannot be distinguished as rational or emotional by judging whether the actor is
or is not aware of his or her behavioral state and action.
The most complex level of emotion involves social
evaluation and assignment of responsibility for actions taken. In the classical Platonic view, in which
reason is apposed to emotion, actions that conform to social standards of
considerate, productive behavior are said to be rational. Actions that appear to lack the prior
logical analysis called premeditation, and that bring unwanted damage to one's
self and others in one's community, are said to be emotional. Yet both kinds of actions are emotional
and intentional, in that both emerge from within the individual and are directed
to short- or long-term goals. They
clearly differ from one another. The biological basis for that difference
lies in the self-organizing properties of brains through which actions are
constrained or deferred by a global self-organizing process. We experience that neurodynamic process
through being aware or conscious. But consciousness does not generate
emotion. It has much more to do
with the control of emotion, and in that respect is closely akin to its
predecessor, conscience ("knowing together").
Understanding emotion at all of these levels depends on an answer to this prior question. How do intentional behaviors, all of which are emotive, whether or not they are conscious, emerge through the self-organization of neural activity in even the most primitive brains?
6
The architecture of stimulus-response
determinism
Most people know the appearance of the human brain,
because it has so often been displayed in popular publications, owing to
widespread interest in brain imaging during normal human behavior. This knowledge can serve to highlight the
differences in emphasis between the passivist-materialist-cognitivist view of
the brain as an input-dependent processor of information and representations
(Figure 1), and the activist-existentialist-pragmatist view of the brain as a
semiautonomous generator of goal-directed behavior (Figure
2).
In the materialist and cognitive conceptions, the
starting point for analysis is assigned to the sensory receptors, either in the
skin (as shown by the *), eyes, ears or other portal at which information from
the world is transduced from energy to action potentials. Bundles of axons serve as channels to
carry the information to the brain stem, where it is processed through nuclear
relays and converged into the thalamus (upward arrows), which is a central
sensory clearinghouse at the top of the brain stem. The information is already subdivided by
the receptors in respect to its features, such as color, motion, tonal
modulation, and so on. The thalamus
sorts it for transmission to small areas within each of the primary sensory
cortices, which are specialized to deal with their designated kinds of
information. Most of the channels
have some degree of topographic order, so that the information is said to be
mapped from the sensory arrays into each of the small cortical
areas.
Within the thalamus, each relay nucleus inhibits the
other nuclei. This is called
competitive inhibition. The nucleus
that is most strongly excited is said to suppress the others around it. These others, being inhibited, fail to
inhibit the excited nucleus, so it is sure to fire. This process is also called
winner-take-all. It is thought to
select information for transmission to the cortex in the process of selective
attention. The hinge that squeaks
the loudest gets the oil.
6
The sensory input is believed to excite receptor
neurons, whose pulses represent the primitive elements of sensation that are
called features. These
representations of features are combined into representations of objects, when
they are transmitted from the primary sensory cortices to adjacent association
areas. For example, the integration
of lines and colors might image a face, a set of phonemes might form a sentence,
and a sequence of joint angles and tissue pressures might represent a gesture.
The representations of objects are
thought to be transmitted from the association cortices to the frontal lobes,
where objects are assembled into concepts, and meanings and value are attached
to them.
The architecture of the motor systems is similar to that
of the sensory systems in respect to topographic mapping, both in the cerebral
cortex and in the cerebellar cortex. Working backward from the muscles along
the downward arrows in Figure 1, the final central relay in the outgoing
channels is provided by pools of motor neurons in the spinal cord and brain
stem. These are driven by networks
of neurons in the basal ganglia, which include a part of the thalamus. At the crest of the chain is the motor
cortex in the frontal lobe, which maintains a topographic map of the
musculoskeletal system. The motor
cortex in turn is controlled by the premotor and supplementary motor areas that
lie progressively more anteriorly. In this view the frontal lobes are the
site of selection and organization of motor activity in accordance with the
objective perception of sensory input.
It is there that the rational information processing selects the
appropriate motor commands that are to be issued through the motor cortex. Emotion is added to color the output
commands by side channels that include the amygdaloid nucleus, which is well
known for its involvement in emotional behavior. Studies initiated 60 years ago by Klüver
and Bucy (1939) showed that bilateral amygdaloidectomy produced hyperorality and
hypersexuality and reduced tendencies to violent behavior in monkeys. The findings led some neurosurgeons to
apply the operation in humans to curb violent behavior in adults (Mark and
Ervin, 1970) and to diminish hyperactivity in children (Narabayashi, 1972).
Extensive experience was then
accumulated on the effects of stimulation in humans (Eleftherion, 1972; Mark,
Ervin and Sweet, 1972). This
structure has recently been given emphasis by imaging studies of the emotion of
fear. In fact, the amygdala is
involved in the expression and experience of all emotions, but it is much more
difficult to elicit and control love, anger, jealousy, contempt, pity, and so
forth in subjects who are immobilized in the machinery that is required for
functional brain imaging. Sex is
problematic, because of the requirement that subjects not move, and the
puritanical attitudes about masturbation in public.
The pathways indicated by the arrows in Figure 1 for the
transmission of sensory information about objects and the motor commands sound
complicated, but the interpretations are based on straight-forward engineering
concepts. They are, in fact, models
that are very well supported by experimental measurements of the pulse trains of
neurons in response to well-designed stimulus configurations. However, these models lead to a number of
unsolved problems. First, the
thalamic winner-take-all mechanism fails to account for expectancy, in which
attention is directed toward a stimulus that is not yet present. Second, the corticocortical pathways that
link the primary sensory cortices to the frontal lobes are well documented, but
no one knows how the features in the small specialized maps are combined to
represent objects, or even how an object is defined. How are the elements, sometimes called
"primitives" by cognitivists, combined to obtain a table and a chair rather than
a chairtable? This is known as the
binding problem (Hardcastle, 1994). It is unsolved. Third, the role of the limbic system is
underplayed and misrepresented. It
is known to be involved with, even required for, spatial navigation, the
formation of explicit memories, and the coloring of motor responses with
emotions. The neural mechanisms by
which the limbic system performs these functions are bundled into "higher
functions" that are to be analyzed after the problems of cognition have been
solved. Fourth, olfaction does not
fit within these architectures and is widely ignored.
7
The architecture of intentional
action
In the activist-pragmatist view (Figure 2) the
organization of the primary sensory and motor systems, which include the
receptors, the muscles, and the dedicated areas of cortex, is accepted as
outlined in the preceding section, but the starting point for analysis is
assigned to the limbic system (*), not the sensory receptors. This is because perception is defined as
a form of intentional action, not as a late stage of sensation. The consequences of this change in
perspective include reassigning the pivotal roles of the thalamus and the
frontal lobes to the limbic system.
In primitive vertebrates the limbic system comprises the
entire forebrain, including naturally both cortical and subcortical structures
as in all definitions of "limbic". The various goal-directed activities that
these free-ranging animals sustain clearly support the assertion that these
animals have limited forms of intentional action. In the human brain the vast enlargement
of the neocortical lobes makes it difficult to see that the primitive components
have not only persisted, but have become enlarged. For example, topologically the
hippocampus still occupies part of the surface of each cerebral hemisphere, but
the folding and twisting of the hemisphere during its embryological growth
relocates it, so it now seems buried deeply within the brain. Although it is only one part of a
distributed system of modules comprising the limbic system, its central location
and characteristic cellular architecture make it a useful focus for
understanding limbic dynamics. In
metaphorical terms, it is more like the hub of a wheel than the memory bank or
central processor of computer.
Whereas in the salamander and other primitive
vertebrates (Herrick, 1948) the hippocampus receives input directly from the
primary sensory areas, in humans and other mammals there is a collection of
intervening cortical areas which feed into the entorhinal cortex. These stages include the inferotemporal
cortex receiving visual input, the cingulate gyrus receiving somatic and other
parietal input, the superior temporal gyrus receiving auditory input, the insula
receiving visceral input, and the orbital frontal region transmitting via the
uncinate fasciculus. The entorhinal
cortex is the main gateway to the hippocampus. It is also the main target for
hippocampal output by way of the subiculum and parahippocampal gyrus, so the two
modules constantly communicate between each other. They occupy the medial temporal lobe of
each hemisphere, along with the amygdaloid nucleus, the orbital striatum, and
the tail of the caudate nucleus.
The most remarkable feature of the entorhinal cortex is
that it not only receives and combines input from all of the primary sensory
areas in the cerebral hemisphere, and it sends its output back again to all of
them, after its previous activity has been integrated over time in the
hippocampus. This reciprocal
interaction in mammalian brains is carried out through multiple synaptic relays
to and from all sensory and motor areas of neocortex. Other pathways support direct
interactions between pairs of these areas, but the most significant aspect of
limbic architecture is the multisensory convergence and integration that
underlies the assembly of multisensory Gestalts, mediates spatial orientation,
and provides the basis for recall of explicit memories (Clark and Squire,
1998).
This architecture of the limbic system is schematized in
Figure 3 as a set of nested loops. The loops have been simplified
deliberately by lumping together many subsidiary components and lesser loops, in
order to show the forest, not the trees. At the core is the space-time loop, which
represents the interaction of the hippocampus with the adjacent neocortex,
mainly the entorhinal cortex. There
are two outstanding properties of this space-time loop. First, the hippocampus has been shown
experimentally to be deeply involved in the orientation of behavior in space and
in time. Cognitivists attribute
these functions to "place cells" (Wilson and McNaughton, 1993). These are neurons that fire pulses
whenever an animal orients itself in a particular place or direction in its
field of action, so they are conceived to provide spatial information for
navigation.
Cognitivists believe that the hippocampus maintains a
cognitive map (Tolman, 1948) and a short term memory bank, which serve to
represent the environment as a part of the world picture within each animal.
Pragmatists hold that there is no
representational "map" in the brain, but that the hippocampal neurons maintains
an experience-dependent field of synapses among its neurons. This field continually shapes and
revises the action patterns that form under the interactions of
the
8
limbic system with other modules in the brain, as the
animal moves through its environment.
Every intentional act takes place in space through time. The space is the personal realm in which
the organism has moved in previous explorations and now continues to move toward
its immediate goals. The time is
the personal lapse that every movement in space requires, and that orders each
sequence of past, present and expected states (Hendriks-Jansen, 1996; Tani,
1996). Intentional action cannot
exist without this learned framework, but it is a dynamic operator, not a
repository of facts or geometric forms.
We experience this kind of navigation in our first exposure to a
The second salient property of this space-time loop is
that the neural populations within its modules have the same and similar kinds
of interconnections and interactive dynamics as those in the primary sensory
cortices. The EEGs generated by
these structures have similar wave forms in time and space, and they show
similar kinds of change with behavioral and brain states as do the sensory
cortices. In the language of
dynamics the populations comprising the space-time loop construct and maintain
an array of "attractors". What this
means is that the limbic system has some preferred patterns of activity, which
tend to recur like good or bad habits or thoughts. Each pattern is governed by an
"attractor" with a "basin" of attraction, called that in analogy to a ball
rolling to the bottom of a bowl to which it is "attracted". The basin is defined by the full range of
conditions of the brain in which the pattern emerges. A collection of patterns is governed by
an "attractor landscape", in analogy to a set of bowls, such that the limbic
system can only be in one at a time, but it can jump from one bowl to another,
hence from one attractor to another. Each jump is the occasion of an
instability. That is, the brain is
continually changing its state, because it is volatile and unstable. Again, there are some preferred pathways
among the basins, which leads to the idea of a pathway or "trajectory", which
supports a habitual pattern of thought and behavior. That emerges as a sequence of briefly
stable patterns, each giving way to the next after its brief moment of life,
coming to awareness as a chain of movements or a familiar train of
thought.
Each attractor provides for a certain brain state, and
the jump from one state to another is called a state transition. These states recur at a rate of 3-7 per
second in the manner of a motion picture film. That is a characteristic frequency of
hippocampal EEG called "theta activity", which is provided by neuron populations
in the septal nuclei and regulated by the brain stem. The spatiotemporal patterns result from
the self-organizing dynamics within the space-time loop (Freeman, 1992). They are shaped and modulated by the
feedback from the larger loops in which the space-time loop is embedded, but the
locus for the critical instabilities that shape the trajectory is located in
this core of the limbic system. It
is the organized and fruitful evolution of limbic patterns through chaotic
instabilities that governs the flow of intentional action (Freeman,
1995).
The dynamics of the motor control
loops
The bulk of entorhinal output goes either to the hippocampus or back to the sensory cortices, but some of it enters into the motor systems. Similarly the bulk of hippocampal output goes back to the entorhinal cortex, but some of it also goes directly downstream. These arrangements reflect a general principle of brain organization, that the larger fraction of the output of each module goes back directly or indirectly to the module from which it gets its input, and only a smaller fraction goes onward.
9
There are two main motor systems that receive and
respond to limbic activity, and that feed back reports about their
contributions. In the lateral side
of each hemisphere in the forebrain a main target is the amygdaloid nucleus
already mentioned. The downward
component of its outflow is directed toward the motor nuclei in the brain stem
and spinal cord (Figure 1) that control the musculoskeletal system through what
is called the "lateral forebrain bundle". In the medial side of each hemisphere the
main targets are the septum, accumbens nucleus and hypothalamus, with relays
into the ventral tegmental area, all of which control the autonomic and
neuroendocrine chemical and metabolic supports for the musculoskeletal system
through what is called the "medial forebrain bundle". These autonomic and hormonal supports are
involved in all emotional expressions, not only in the periphery where their
effects are visible to everyone, but also inside the brain itself. The internal ascending pathways from the
brain stem that diverge broadly through the cerebrum are well documented. A more recent development is a better
understanding of how brain tissues use neurohormones to regulate their own blood
supply. The consequences of the
changes that these systems bring about in the function of the body cannot fail
to alter the sensory input from the proprioceptor neurons in the muscles and the
interoceptor neurons in the viscera, which operate concomitantly with the
exteroceptor neurons in the eye, ear and skin, and continually influence the
somatosensory areas of the forebrain, including the thalamus and cortex. Considering the rapidity with which an
emotional state can emerge, such as a flash of anger, a knife-like fear, a surge
of pity or jealousy, whether the trigger is the sight of a rival, the
recollection of a missed appointment, an odor of smoke, or the embarrassing
rumble of one's bowel at tea, the occasion is best understood as a global state
transition involving all parts of the brain and body acting in concert. Of course, onsets can also be gradual.
However, this description of the
dynamics does not yet serve to distinguish between, for example, the quale
experienced in aerobic exercise from the quale of hot pursuit. There is more to
emotion than the limbic system.
What role does the motor cortex in the frontal lobe have
in this schema? The limbic output
goes from the amygdaloid nucleus into other parts of the basal ganglia, and from
the hypothalamus into the thalamus. By these routes limbic control is broadly
established in the frontal lobe, which is motor in two senses. In the narrow sense the primary motor
cortex (Figure 1) controls the position of the limbs, and also of the head and
eyes to optimize the sensory inflow in accordance with the goal-directed actions
that are initiated in the limbic system. It does not initiate the actions nor
formulate their intents.
In the broad sense the frontal lobe constructs and
elaborates the predictions of future states and possible outcomes toward which
intentional action is directed. In
primitive animals there is little or no frontal cortex, and their intentional
action is correspondingly impoverished. Even in cats and dogs, and in
large-brained animals such as elephants and whales, the frontal lobe comprises
only a small fraction of each hemisphere. These animals are short-sighted and have
brief attention spans. The great
apes presage the emergence of the dominance of the frontal lobes in humans.
Two aspects are noteworthy. The dorsal and lateral areas of the
frontal lobe are concerned with cognitive functions such as logic and reasoning
in prediction. The medial and
ventral areas are concerned with social skills and the capacity for deep
interpersonal relationships. These
contributions can be summarized as foresight and insight. The frontal lobe guides and elaborates
intentional action but does not initiate it. In respect to emotion, it provides the
operations that distinguish between pity and compassion, pride and arrogance,
humility and obsequiousness, and so on in an incredible range of nuances of
feelings and values. The tale has
often been told, most recently by Damasio (1994) of the emotional impoverishment
of Phineas Gage by damage to his frontal lobes.
A remarkable feature of the human brain is a fact that
embodies the principle noted above of the dominance of feedback (recursion,
re-entry, self-activation) in brain architecture. This is immediately apparent on
inspection of the organization of neurons in all parts of the brain. Each neuron is embedded in a dense fabric
of axons and dendrites, which is called "neuropil", in which its thousands of
connections form. Most of the
connections for each neuron are from others in its
10
neighborhood, but about 10% come from distant
structures. For example, the
frontal lobes provide about 80% of the descending axons from the forebrain into
the basal ganglia and brain stem, but only a small fraction reaches the motor
nuclei. Virtually all of the output
of the basal ganglia goes back to the cortex, either directly or through the
thalamus. Virtually all of the
output of the brain stem goes back to the cortex, through the thalamus or the
cerebellum. These massive internal
feedback pathways are crucial for learning, practice, rehearsal, and play in
forming the detailed structure of experience, which is the history of the
organism that provides the wholeness and richness of texture that is unique to
each individual. This texture
provides the unique quale of emotion in each of us, which is our inner
experience of impending action. If
the classes of such action are reduced to the dichotomy of approach versus
avoidance, then the experience of feeling can be reduced to the bivalence of
pleasure versus pain, but that simplification leaves out the options of
deferring action, of declining to act, of weaseling around in search of angles,
or perhaps of just seeking more information. Curiosity can inspire growing dread of
what will be found. Who can stop
before it is too late?
Undoubtedly these large, strongly interconnected populations have the capacity for self-organizing nonlinear dynamics, comparable to those of the primary sensory and limbic modules. They are active participants in shaping the complex behaviors in which humans excel, far beyond the capacities of even our closest relatives among the great apes. What is important in this context is the dynamics that we share with our closest and also our more distant relatives (
The neurohumoral dynamics of
emotions
An essential part of the motor systems is found in the
brain stem of all vertebrates, from the simplest to the most advanced. This a collection of nuclei with neurons
that are specialized to secrete types of chemicals that are called
neuromodulators. Whereas
neurotransmitters are chemicals released at synapses that immediately excite or
inhibit the postsynaptic neurons, the neuromodulators enhance or diminish the
effectiveness of the synapses, typically without having immediate excitatory or
inhibitory actions of their own, and typically effecting long-lasting changes in
the strengths and durations of synaptic actions. The nuclei are arranged in pairs on both
sides of the brain stem, extending from the hindbrain into the base of the
forebrain, everywhere embedded in the core of the brain stem, the
centrencephalic gray matter, the reticular formation (Magoun
1962).
These nuclei receive their input from many parts of the
sensory and motor systems of the brain.
Most important is the limbic input to these nuclei that modulates the
emotion of intentional action.
There are several dozen neuromodulators, which are grouped in two main
classes based on their chemical structure: the neuroamines and the neuropeptides
(Panksepp, 1998; Pert 1997). The
axons of these modulatory neurons typically branch widely and infiltrate among
neurons the neuropil without making terminal synapses. They secrete their chemicals that
permeate throughout both cerebral hemispheres. Their actions are global, not local.
This functional architecture is a
major determinant of the unity of intentionality, because the entire forebrain
is simultaneously affected by the action of each pair of nuclei. To some extent the differing nuclei
interact by competitive inhibition, which may enhance winner-take-all capture of
the forebrain by the nuclei.
The types of modulation include generalized arousal by
histamine; sedation and the induction of sleep by serotonin; modulation of
circadian rhythms by melatonin; the introduction of value by the reward hormone
cholecystokinin, CCK; the relief of pain by the endorphins; the release of
aggressive behavior by vasopressin; the enabling of the appearance of maternal
behavior by oxytocin; and the facilitation of changes in synaptic gains with
imprinting and learning by acetylcholine and norepinephrine (Gray, Freeman and
Skinner, 1986), which is crucial for updating intention in the light of the
consequences of previous actions; and dopamine that is
11
involved with control of energy level and of movement as
in exploratory behavior and the initiation of new projects (Panksepp,
1998).
The changes in synaptic strengths with learning, as
mediated by neurohormones, are not restricted to a particular sensory modality
or motor system, where a particular conditioned stimulus (CS) evokes a
particular conditioned response (CR). In conformance with the unity of
intentionality the changes occur everywhere in the forebrain that the
simultaneous activity of pre- and postsynaptic neurons meets the conditions for
Hebbian learning, in which the strength of synapses is modified by the
activities of the neurons simultaneously on both sides of the synapse. They are also cumulative, which meets the
requirement for continuing additions to the personal history constituting the
evolving wholeness of intentionality. When a new fact, skill or insight is
learned, the widespread synaptic changes knit the modification into the entire
intentional structure of meaning that is embedded in the
neuropil.
Neuromodulators combine their actions in the states of
people and animals that we describe in terms of mood, affect, mania, depression,
and so on. It is not clear how
these complex interactions take place, or how the modulators are related to
specific emotions of individuals, as they are experienced through awareness, but
it is certain that all of them are involved in expressing emotions and learning
from experience.
The dynamics of the preafference loop
When internally organized action patterns radiate from
the limbic system, they are not packets of information or representational
commands as empiricists or cognitivists would describe them. They are solicitations to other parts of
the brain to enter into cooperative activity, by which the spatiotemporal
patterns of both the initiator and the co-participants engage in a kind of
communal dance. The linking
together in a global pattern is not a directive, by which the limbic system
imposes a predictive schema onto the motor systems. It is a process of evolution by
consensus, in which each of the sensory and motor modules makes its unique
contribution. Each sensory module
provides a porthole through which to view the world, which is specified by its
receptor neurons. The motor modules
provide the linkage through the motor neurons to the movers of the body and the
metabolic support systems. For the
limbic system the contributions are the spacetime field, the feedback regulation
of the neuromodulator nuclei in the reticular core, and the simultaneous
integration of the input from all of the sensory areas, which establishes the
unity of perception. That
integration provides the basis for the synthesis of intent.
All of the solicitations for cooperation radiating to
the motor systems are simultaneously radiated to all of the primary sensory
cortices through the bidirectional connections schematized in
Figure 3. The existence of these influences into
other parts of the brain has been postulated for over a century. The transmissions have been called
efference copies and corollary discharges. They are highly significant in
perception, because they provide the basis on which the consequences of
impending motor actions are predicted for the coming inflows to each of the
sensory ports in the process of preafference (Kay and Freeman, 1998). When we move our heads and eyes to look,
this process tells us that the motion we see is in our bodies and not in the
world. When we speak, this process
tells us that the voices we hear is our own and not others'. Preafference takes place entirely within
the brain. It is not to be confused
with the proprioceptive loop, which feeds through the body back to the sensory
receptors and the somatosensory cortex.
Corollary discharges are carried by action potentials,
as are virtually all corticocortical transmissions, with a subtle but
significant difference from forward motor transmissions. The spacetime loop has two directions of
both inflow and outflow. In my view
the forward flow in from the sensory modules and out to the motor modules is
carried by spatiotemporal activity patterns that are carried by pulses, whose
effects are at the microscopic level to direct their targets into appropriate
attractors. The feedback flow from
the motor modules to the limbic system and on to the sensory modules as
corollary discharges is also carried by activity patterns of pulses,
but
12
their effects are at the macroscopic level, to serve as
order parameters, shape the attractor landscapes, and facilitate the selective
learning that characterizes intentionality (Freeman,
1995).
Preafference in the forebrain has even more important
contributions to make. When a
goal-directed state emerges by a nonlinear state transition with its focus in
the limbic system, it contains within it the expectancy of a sequence of sensory
inputs. Those anticipated inputs
are highly specific to a planned sequence of actions along the way to achieving
the specific goal, as well as to a future state of reward, whether it is food,
safety, or the feeling of power and comprehension that accompanies activation of
the dopamine receptors. These
expected inputs are the sights, sounds, smells and feels of searching and
observing. The organism has some
idea, whether correct or mistaken, of what it is looking for. The scent of prey combined with the touch
of wind on the skin instantly involves the ears to listen and the eyes to look
for waving grass. These are the
Gestalt processes of expectation and attention, which are sustained by the motor
control and preafference loops.
Without preconfiguration, there is no perception. Without sensory feedback, there is no
intentional action.
Everyone agrees that central processing takes time,
whether for information, representations, or intentional states. Minimal estimates are provided (Libet,
1994) by measurements of reaction times between CSs and CRs (about 0.25 to 0.75
second), which are longer than the reaction times between unconditioned UCSs.
and UCRs (less than 0.1 second). Only a small fraction of this interval is
taken by the conduction delays between receptors and the brain, between the
brain modules, and from the brain to the muscles. Most of the interval is required for
binding features into higher order brain states, or for retrieving and matching
stored representations for cross-correlation with present input, or for seeking
appropriate basins of attraction and constructing spatiotemporal patterns in an
itinerant trajectory, depending on one's point of view.
Neocortex as an organ of mammalian
intentionality
Recent findings by recording the EEGs from the scalp of
human volunteers (Lehmann, Ozaki and Pal, 1987) indicate that cooperation
between the modules in each hemisphere is not by sequential transmission of
information packets or representations bouncing from one area to another, with
local processing by computational or logical algorithms. That hypothesis might be compared to the
response of billiard balls upon the impact of the cue stick on one of them, with
the outcome being determined by Newtonian dynamics. The global spatiotemporal pattern
formation revealed by EEG recording shows that the sensory and limbic areas of
each hemisphere can rapidly enter into a cooperative state, that persists on the
order of a tenth of a second before dissolving to make way for the next state.
The cooperation does not develop by
entrainment of coupled oscillators into synchronous oscillation. Instead, the cooperation depends on the
entry of the entire hemisphere into a global chaotic
attractor.
An explanation in terms of brain dynamics is through
generalization of the process by which local spatiotemporal patterns form. The microscopic activity of the neurons
in each sensory cortex couples them together by synaptic transmission, and when
the coupling is strong enough, the population becomes unstable and undergoes a
state transition. Thereby a new
macroscopic state emerges, which constrains and enslaves the neurons that create
and sustain it, in the process of circular causality (Haken, 1983; Cartwright,
1989). The neurons express their
membership in the coordination of their firing patterns, even though they do not
synchronize to fire simultaneously. It appears that the macroscopic patterns
radiate through various axonal pathways in each hemisphere. The interactions on the global scale
engender state transitions of the entire hemisphere by triggering instabilities,
such that new global macroscopic states are continually being created. Each global macroscopic state constrains
and enslaves the modules that have created it throughout the
hemisphere.
13
Consciousness as a dynamic
operator
Neurodynamics offers a new and enlarged conceptual
framework, in which interrelationships among parts creating wholes can be
described without need for causal agents to effect changes. An elementary example is the
self-organization of a neural population by its component neurons. The neuropil in each area of cortex
contains millions of neurons interacting by synaptic transmission. The density of action is low, diffuse
and widespread. Under the impact of
sensory stimulation, or by the release from another part of the brain of a
modulatory chemical, or by the inevitable process of growth and maturation, all
the neurons together form a macroscopic pattern of activity. That pattern simultaneously constrains
the activities of the neurons that support it. The microscopic activity flows in one
direction, upward in the hierarchy, and simultaneously the macroscopic activity
flows in the other direction, downward. With the arrival of a new stimulus or
under the impact of a new condition, this entire cortex can be destabilized, so
that it jumps into a new state, and then into another, and another, in a
sequence forming a trajectory. There is no meaning to the question, how
individual neurons can cause global state transitions, any more than it is
meaningful to ask how some molecules of air and water can cause a hurricane.
This way of thinking about matter
has become so familiar to physical scientists since it was introduced a century
ago by Boltzmann, that it is difficult to see why it is not better understood by
neurobiologists working with neurons.
The primary sensory cortices are also components in a
larger system, together with the various parts of the limbic system. Each of these components is liable to
destabilization at any time, in part because of the feedback connections that
support the interaction between populations. Perception can and does follow the impact
of sensory bombardment, but that which is perceived has already been prepared
for in two ways. One way is by the
residue from past experience, the synaptic modifications, which shape the
connections in the neuropil of each sensory cortex to form nerve cell
assemblies. Each assembly opens the
door to a preferred spatial pattern, which is constructed by the learned
attractors in the basin formed in the past. The set of basins forms an attractor
landscape. The second way is by
reciprocal relations with all other sensory cortices through the entorhinal
cortex. Input by preafferent
pathways can bias the attractor landscapes of the cortices, and that can enhance
the basins of attraction, that conform with the goals emerging through the
limbic system.
The sensory cortices are continually bombarded by
receptors, irrespective of intention, and each module of the brain is subject to
destabilization at any time, owing to its intrinsic dynamics. Some form of global coordination must
exist to explain the unity of intentional action, and the perseverance of
goal-directed states in the face of distractions and unexpected obstacles. My hypothesis is that the interactions of
the neural populations creates a brain-wide level of shared activity. The populations are not locked together
in synchronous discharge, because they preserve a degree of autonomy. Synchrony seldom occurs among the
individual neurons in the local populations, either. The entire community of brain modules
must be considered as creating a global dynamic framework. The micro-macro relation that binds
single neurons into populations, then, is a precursor for the binding of the
limbic and sensory systems into a brain state.
This description can explain the formation of global
spatiotemporal patterns but not their function and significance. It still leaves unexplained their
relation to awareness. What is it?
I want to propose a hypothesis as
to just what is going on, in which consciousness is interpreted in
neurobiological terms as a sequence of states of awareness. The limbic and sensory systems transmit
to each other by action potentials as microscopic elements in a hierarchically
upward direction. They create a
global state, which acts downwardly to constrain the parts. The constraints are exercised by action
potentials on divergent pathways that enhance the global content. The constraint of each module acting on
others diminishes the freedom of all of them. The likelihood that any one of them will
destabilize, go ballistic, and impose its activity onto other modules is
reduced. In particular, it is less
likely that any one or a subset of modules can capture the motor systems and
shape behaviors with minimal contributions from the other
parts.
14
My hypothesis is that a global spatiotemporal pattern in
each hemisphere is the principle brain correlate of awareness. The interactive populations of the brain
are continually creating new local patterns of chaotic activity, that are
transmitted widely and that influence the trajectory of the global state. That is how the contents of meanings
emerge and grow in richness, range, and complexity. Only a small fraction of the total
variance of the activity in each of the modules is incorporated into the global
pattern. Yet that small part is
crucial. Just as the individual
neuron is subject to continual bombardment at its synapses, yet can only report
out a pulse intermittently on its sole axon, and just as the population is built
from the seemingly random activity of millions of neurons, yet can only form one
attractor pattern at a time, so the whole hemisphere, in achieving unity from
its myriad shifting parts, can sustain only one global spatiotemporal pattern at
a time, but that unified pattern jumps continually, giving the chaotic but
purposeful stream of consciousness.
The crucial role that awareness plays, according to this
hypothesis, is to prevent precipitous action, not by inhibition, but by
quenching local chaotic fluctuations in the manner described by Prigogine,
through sustained interactions acting as a global constraint. Thus awareness is a higher order state,
that harnesses the component subsystems and minimizes the likelihood of renegade
state transitions in them. Consciousness as a sequence of global
states is not an agent that initiates action. Nor is it an epiphenomenon. It is a state variable that constrains
erratic activity by quenching local fluctuations. It is an order parameter and operator,
that comes into play in the action-perception cycle after an action has been
taken, and during the learning phase of perception. This is the part of intentionality in
which the consequences of the just completed action are being organized and
integrated, and a new action is in planning but not yet in execution. Consciousness holds back on premature
action, and by giving time for maturation, it improves the likelihood of the
expression in considered behavior of the long term promise of an intentional
being and of the expression in considered behavior of the long term promise of
an intentional being. David
Chalmers (1996) has characterized as "the hard problem" the question of why we
have experience at all. The answer
is simple. Humans who can't stop to
think don't survive long in competition with those who can. William James (1879) described
consciousness as "an organ added for the sake of steering a nervous system grown
too complex to regulate itself." But it is not an organ in the sense of
some new part of the brain. Instead
it is a higher and more inclusive form of
self-organization.
The view of consciousness as a dynamic state variable
clarifies the issue of emotion versus reason. Emotion can be measured by the
magnitudes of the tendencies to chaotic fluctuations in brain modules, and
reason can be seen as an expression of a high level of assimilation to the
world, meaning knowledge that endows a rational mind with control of remarkable
power. Consciousness does not
construct the trajectory of reason. It provides the global linkage for
smoothing chaotic fluctuations through global interaction. By these criteria an action can be
intensely emotional and yet strictly controlled. Actions which are considered to be
thoughtless, ill-conceived, rash, incontinent, inattentive, or even unconscious,
and which are commonly and incorrectly labeled as "emotional", can be described
in dynamic terms as an escape of chaotic fluctuations from a global order
parameter, prematurely in respect to unity of mind and long-term growth toward
the wholeness of intentionality. Without emotion there is no action, but
without conscious control, there is the potential for self-abasement,
self-destruction, and the heartless infliction of violence on
others.
When we speak of people as "highly emotional", in this
view we refer to having high levels of chaotic activity in the various
components of their brains, which cannot be achieved without a corresponding
high level of the global cooperativity that manifests itself in consciousness.
The levels of energy build
inexorably through the dynamic tensions of controlled internal conflicts. In other words, emotionality is not a
weakness but a sign of strength, because its depth, range and complexity beyond
the instinctual attitudes of other animals cannot develop without structuring by
reason and language. The highest
and most complex levels of emotion are seen in poets and other natural leaders
who have the greatest range of personal insight, cultural vision, and predictive
power. Emotion is chaotic, but,
after all, by one definition chaos is controlled noise.
15
This work was supported by a grant from the National
Institute of Mental Health entitled "Correlation of EEG and Behavior". Much of the material here has been
adapted from a chapter in a forthcoming monograph tentatively entitled "The
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