Somatic Sensation

10/16/01

S. David Stoney, Ph.D.

Towards an Ecological Neuroscience - Somatic Sensory System

"The emphasis on action and adaptation is closely connected to the assertion that there is intrinsic affect in sensation. Affect can incite action (a tendency to approach or avoid), but it is unclear how awareness alone or a mere registering of a thing without evaluation, could result in adaptive behavior." (Wayne Viney, Charles Hartshorne's philosophy and psychology of sensation, In: The Philosophy of Charles Hartshorne, The Library of Living Philosophers, Volume XX, Lewis Edwin Hahn (Ed.), LaSalle, IL: Open Court, pg. 105, 1991.)

I. A New Somatic Sensory Neuroscience

A. Introduction. The old view of somatic sensory neuroscience is that the neurons of the brain generate "representations" of objects in the external world <1>, which - when the neurons are electrically active - the mind somehow perceives. The utility of the notion of representations for the identist (mind = neural activity) point of view is obvious. If neuronal activity "represents" (in the sense of 'making a copy of') the world and if that same activity "is" the mind, then one can justifiably claim that the mind-body problem is close to being solved: by knowing our neurons we know (a representation of) the world. This gives us, however, as Santayana said, "solipsism of the present moment," where each of us is completely alone, encased within our own skull, contemplating our neuronal representations without any notion of past or future. Furthermore, the hard problems - of how neuronal electrical activity leads to conscious awareness and why the matter that makes up neurons in certain parts of the brain allows awareness to occur whereas no other kind of matter does the same - remain unsolved.

The new view proposes that the somatic sensory system "represents" (in the sense of 'making clear') for the mind the-body-in-contact-with-the-world. This view accepts that everything is interconnected at the level of quantum nonlocality (nonsensory perception; Hartshorne's "affective continuum," see <6>) and that having a nervous system allows us to become consciously aware of those aspects of the world toward which we have intention, regard, or concern, i.e., which afford us opportunities for action. In this view, there is no need for the brain to represent (create an image of) the world since we already "know" it - we are literally part of it - at a preconscious level. It seems to me that this process philosophical approach also solves what I call the "representation problem." This problem is an empirical one, namely, as will be briefly described below, that there are no neurons in the brain that can be said to actually represent (stand for) the world or its objects, at least not in any way that is discernable to a human observer monitoring their activity. I should add, for the sake of completeness, that even though the process philosophical approach appears to solve the "representation problem," there still remains a pretty hard problem of why and how neuronal electrical activity is necessary for embodied human consciousness. I suspect we will make more progress on that issue once we abandon the mistaken notion that the role of neuronal electrical activity is to generate internal representations of things.

B. The features of receptive fields of somatic sensory neurons support the idea that neuronal activity signals prehensions. Each neuron in the somatic sensory system has a receptive field (RF) and is active (firing action potentials) when we handle, or are touched by, or imagine (for neurons > 1st order) handling an object that contacts the RF.

Up to and including the level of SI cortex (areas 3b and 1), neurons have simple contact-sensitive RFs, generally similar to the RFs of first order fibers, except that they are somewhat larger and have an additional "inhibitory surround" component. In area 2 of SI cortex and in areas 5 & 7 of the posterior partial cortex, neurons have more complex receptive fields. Four types of neurons have been discovered that are considered to be "feature detectors," which are thought to "represent" larger, or more behaviorally relevant 'chunks' of the world and its objects. These include

Orientation-sensitive neurons that respond with selectivity to the orientation of a linear object pressing on the skin.
Direction-sensitive neurons that respond with selectivity to the direction of movement of a tactile stimulus across the skin.
Texture-sensitive neurons that respond with selectivity to the texture (rough vs. smooth) of an object
Shape-sensitive neurons that respond with selectivity to different objects that are grasped in the hand.

The figure below, copied from Kandel, Schwartz, & Jessel, Principles of Neuroscience, 4th Edition, 2000, illustrates the typical response pattern of a "feature detector" neuron, in this case a direction sensitive neuron.

[I don't have, at the moment, good pictures of response patterns of texture or shape-sensitive neurons. However, the comments that follow apply to them just as well as to the illustrated response patterns.] Note in particular that the neuron is not uniquely sensitive to stimuli of only one direction of movemnent. Instead, the neuron responds fairly vigorously to a range of stimuli; it is broadly tuned with regard to the details of stimulus features. In fact, for all "feature detector" neurons that I am familiar with, including neurons in motor cortex important for voluntary movements, the stimulus - response function is like that shown in the figure below. Although one "feature" causes the greatest response (highest frequency of firing), other, different, features also cause vigorous responses. What grounds, other than wishful thinking, exist for deciding that the neuron "represents" stimulus 4 but not stimulus 3 or 5? Data such as this seems to indicate that no single neuron uniquely signals (represents) a particular stimulus feature, much less all the features so as to represent the stimulating object.

In fact, in no instance that I have become aware of in over forty years of learning about how neurons respond to somatic stimuli <2>, has any neuron, any where in the brain been shown to uniquely represent an object (or anything else). In every case, neurons sensitive to somatic sensory stimuli (objects touching the skin, etc.) simply respond when the object touches, or enters, the RF. This is true even for the neurons in the tertiary somatic sensory (a.k.a. "association") cortex of the inferior parietal lobe, as well as for some neurons in premotor cortex and the putamen of the basal ganglia, that have some of the most complex RFs currently known. Such a neuron responds to touch of a body part, e.g., the left cheek (a classical touch-sensitive RF) and to a visually observed object moving toward the animal on a trajectory that will bring it to or close to its cheek (a visual RF shown by the outlined space lateral to the animal's jaw ).

Such a neuron has a cutaneous and a movement-sensitive visual RF. The figures below (taken from <3>), illustrates similar RFs for other neurons in the putamen of an anesthetized monkey. On the left, neurons had overlapping tactile + visual RFs involving the upper extremities. On the right, a neuron had a visual RF to the right only when the arm was in an upward position where it entered (overlapped) the visual RF! The conventional (neuralist) explanation of the meaning of such RFs is that such neurons "represent" the animal's nearby extrapersonal "space" in body-centered coordinates.

Well, perhaps so; however, my mind keeps slipping off the notion of a neuronal RF representing such a high-level abstraction as "space." What if the process philosophical approach is correct and there is, in fact, no need for the brain to "represent" (stand for) the world, its objects, or space? In that case the situation is incomparably simpler: From a process philosophical perspective, what all these neurons we have considered are quite clearly doing is signaling the establishment of a connection between the organism and the object (stimulus) in the environment. These neurons are signaling the establishment of what Alfred North Whitehead called a "prehension" between the subject and the object. What is (in a sense) already known at a non-cognitive, nonlocal level (nonsensory perception in the mode of causal efficacy; interior feeling; affect) is in the process of becoming known at a sensory level (perception in the mode of presentational immediacy; exterior appearance); and the knower, the object of knowledge, and the act of knowing are, for the duration of the experiential event, a unitary whole. Thus, these neurons do not "represent" (in the sense of "standing for") the world and its objects so that the mind may know them. Instead, these neurons, when active, oscillate the world and its objects into awareness, and that awareness is necessarily conscious and embodied. That is, they "represent" (in the sense of "make clear for the mind") the nature of the object from an embodied perspective.

The fact that these neurons in the putamen, a part of the brain not noted for its contributions to conscious sensory awareness, were recorded in an unconscious (anesthetized) monkey raises some questions. I would argue (and will do so in more detail later, in conjunction with the motor system lectures) that these neurons are part of a process that signals potential, not actual, conscious events. The total set of such neurons and their sensitivities will define the motorsensory horizon, just what aspects of the world and its objects any particular creature will potentially be able to perceive and take action toward. When the animal makes an action decison (which presumably would not be possible for an anesthetized animal), the experience of a subset of such neurons, and the neurons in other parts of the somatic sensory system with which they are in prehensive relation, will be bound together and an agent, taking action in the world blossoms into an occasion of conscious awarenss.

II. Solving the "binding problem" seems to require neuronal prehension. Neuralists claim to circumvent the "representation problem," but in so doing seem to invoke the idea of neuronal prehension without knowing it. They argue that, while it is true that no neuron uniquely represents anything, the response of the whole population of neurons, each of which vaguely represents one or another stimulus feature, contains very specific information. "Population codes" or "distributed codes," they say, uniquely represent each and every stimulus. This gives rise to the "binding problem," namely how is the activity of spatially separate, not anatomically interconnected neurons that represent one or another stimulus feature brought together, or integrated (bound up), into a knowing of a whole object? In short, how is the information encoded in the population assessed? The answer, according to the neuralists, is to be found in synchronous neural firing. When spatially separate neurons fire action potentials at nearly (within ~ 1 msec) the same time, their information is, somehow, unified into a whole percept. Esther Gardner and Eric Kandel, near the end of their chapter on "Touch" in Principles of Neural Science describe the situation as follows:

"How does the brain put together all of these features to form a coherent percept of an object? The firing patterns of neurons in separate cortical areas interact in ways we do fully not understand. The problem of binding together activity in different regions of the cerebral cortex has been studied more extensively for vision than for touch. Those studies of the visual system indicate that the brain may bind together the various stimulus features by synchronizing firing in different cortical areas." (pg. 468)

Now please make no mistake about two well-established empirical facts: Population responses do contain very specific information and synchronous neural firing is widespread in the brain (not just the cortex) during conscious perception<4>. Those facts are not an issue. The issue is how synchronous neural firing causes binding. From the neuralist perspective, saying that "neurons that fire together represent together" seems like a magical explanation, somewhat equivalent to a statement like, "Well, that is just the way the mind works; it can pick and choose which neurons it wants to pay attention to." In contrast, from a process philosophical perspective, the ubiquitous presence of synchoronouly firing neurons in the brain during conscious awareness fits right in. That is, prehensive networks of neurons, whose electromagnetic oscillations are to establish the content of conscious awarenss from an embodied perspective, fire synchonously. By definition, the information content of a prehensive neural network is bound! Thus, from a process philosophical perspective it appears that there is no such thing as a "binding problem."

III. Body Schema. A similar process is going on all the time with the body via proprioception. In fact, our somatic sensory perceptual system prehends (many of) the cells of the body and it is only because of this "feeling of feeling" of the cells of our own body that we are able to come to know our own body in the world. This is what accounts for our so-called "body schema" (an illusion of 'folk empiricism') and the posterior parietal/superior temporal lobes of the right hemisphere seems to be particularly important in this regard. There is suggestive evidence <5> that supports the idea that the right infereior parietal/superior temporal cortex is especially important for non-sensory processing. See "Prehensive Networks and Conscious Awareness" for further considerations of the idea of body schema.
See Anosognosia for Hemiplegia for a recent attempt to use the notion of two varieties of perception to explain a mysterious condition that seems to involve a loss of one half of the body schema. This condition sometimes follows a right hemisphere stroke that involves the parietal lobe. The anosognosic patient denies that he or she is paralyzed and neglects stimuli to the left side of the body.

IV. The Locus of Somatic Sensory Awareness. What is true for somatic sensation is probably true for the other senses. The senses share a common logic of operation: objects that have been prehended and which afford an opportunity for action blossom into sensory perception. For compound individuals with nervous systems, the locus of conscious perceptual awareness is, of course, the dominant occasion of experience, also known as "the mind." Unfortunately, the ease with which 'mind,' as the experiential, i.e., "mental" capability of the dominant occasion of experience, can be abbreviated or circumscribed (reified) into a thing-like entitiy inhabiting ordinary bits of the world as they are known to us via sensory perception causes enormous problems. The neural dependence of embodied conscious awareness compounds these problems. Together, these snares are likely to lead astray those who are not wary of the "fallacy of misplaced concreteness," causing them to fall prey to the mistaken notion that mind is simply "in" the brain or "in" the activity of certain neocortical neurons. This is a very hard belief to eliminate in part because it seems so commonsensical, after all, the substantiality of matter is a fact of daily experience and consciousness depends on brain activity. Another reason it is a hard belief to give up is that it is partly true – mind is "in" the brain, in the sense that we are beholden to properly working brains for the content of our embodied consciousness. Nevertheless, such a point of view is far from the complete picture. Mind is, in fact, a distributed function of brain, body, and world: it is as correct to say that mind is "in" the body, or "in" the world, as it is to say that it is "in" the brain.

To put mind just into brain is, in part, to succumb to the representationist fallacy, the mistaken belief that the brain must – and does – generate internal representational standins, i.e., images, signs, symbols, or some other substitute, for the external world and its objects in order for us to become consciously aware of them. Obviously, these problems can be avoided by adopting a panexperiential (process philosophical) perspective.

V. Notes and References

1. Consider, for example, this section heading in the Chapter on "Touch" by Esther Gardner and Eric Kandel in the Principles of Neural Science, 4th Ed.:

"The Body-Surface is Represented in the Brain by the Somatotopic Arrangement of Sensory Inputs." (Italics added.)

Or take Pashler's description of the sensationist approach:

"The core idea of the information-processing approach is to analyze the mind in terms of different subsystems that form, retain, and transmit representations of the world. The nature of these subsystems, the kinds of transformations they carry out, and the temporal relationship and relative discreteness (or nondiscreteness) of their activities are all viewed as facts to be discovered, not assumed at the outset. Obviously, one cannot say in advance whether or not the mind can be successfully analyzed in these terms." Harold E. Pashler, The Psychology of Attention, Cambrige, MA: The MIT Press, pg. 7, 1998.

Or take another example from Principles of Neural Science:

"Our sensory systems form internal representations of our bodies and the external world. One of the principle functions of these internal representations is to guide movement. Even a simple task such as reaching for a glass of water requires visual information to establish an internal representation of the location of the glass in space. It also requires proprioceptive information to form an internal representation of the body so that appropriate motor commands can be sent to the arm... [For voluntary movement t]he task of the motor systems is to reverse the task of the sensory system. Sensory processing generates an internal representation of the world or the state of the body, but motor processing begins with an internal representation, namely the desired result of movement." Principles of Neural Science, 4th Ed., (Kandel et al, Eds), New York: McGraw-Hill, pgs. 651 & 658, 2000.

2. Asanuma, H., Stoney, S.D., Jr., and C. Abzug, Relationship between afferent input and motor outflow in cat motorsensory cortex. J. Neurophysiol. 31:670-681,1968.

3. Graziano, M.S.S. and C.G. Gross, A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields, Exp. Brain. Res. 97:96-109, 1993.

4. For example, see Llinas, R. and D. Pare, The brain as a closed system modulated by the senses, In: The Brain-Mind Continuum: Sensory Processes, Cambridge, MA: The MIT Press, pgs. 1-18, 1996; Nicolelis et al, Simultaneous encoding of tactile information by three primate cortical areas, Nat. Neurosci. 1:621-630, 1998.

5. Deouell, L.Y., Bentin, S., and N. Soroker, Electrophysiological evidence for an early (pre-attentive) information processing deficit in patients with right hemisphere damage and unilateral neglect, Brain 123: 353-65, 2000. See also Karnath, Hans-Otto, New insights into the function of the superior temporal cortex, Nature Revs. Neurosci. 2: 568-76, 2001.

Last modified 10/16/01