S. David Stoney, Ph.D.

Role of Inhibition in the Formation of Somatic Sensory Prehensive Neural Networks

"What is not disallowed may become actual"

"According to CNT, each creature is a more or less passive recipient of sensory input that leads, more or less directly, to a response.  To the contrary, we now realize that the brain, being first and foremost a device for motor control, has much more of a selection function on what is to be consciously perceived."
"To label an object with a certain kind of concept is to mark in precise terms the kind of action or attitude the object should suggest to us.  All knowledge, properly so called, is then oriented in a certain direction, or taken from a certain point of view.
(Henri Bergson, An Introduction ot Metaphysics, NY: G.P. Putnam's Sons, pg. 41, 1912)

[Note: This is still quite rough. The idea I intend to develop is that neural prehensions, which generate potential prehensive neural circuits, occur during periods of neural quiescence, i.e., during periods of inhibition. Conscious awareness blossoms when one of the potential prehensive neural circuits explodes into electrochemical activity.]

I. Introduction. According to the view of classical neural theory (CNT), inhibitory synaptic processing is the hand-maiden of excitation.  Supposedly, excitation does the "real" work of the brain which inhibition works in the background, or off to the side, keeping things under control in a passive sort of way, sharpening the archipelagoes of excitation into meaningful islands (patterns) representing objects.  At the risk of generating a caricature, this view might be described by the phrase, "What fires together, represents together."  As will become more apparent when we consider the motor systems of the brain, the process philosophical approach suggests a more fundamental and important role for inhibitory processing.  This view, which is discussed below with regard to the somatic sensory system, might be described as "What is not disallowed from firing together, may represent together."

II. Ubiquitous inhibitory processing.  There is no part of the nervous system, not the retina of the eye, the organ of Corti in the ear, the olfactory bulb, enteric plexuses of the gut, the simplest reflex arcs of the spinal cord, or anywhere else, where inhibitory neurons are not present and active.  Quite rightly and correctly, inhibitory processing has been seen as having a role in "shaping" excitatory processes.  This is certainly a real and important role, for if inhibitory processes in the brain are blocked, it rapidly goes into potentially fatal, paroxysmal storms of unchecked excitation.  However, CNT does a dis-service to the importance of inhibition in thinking of its role as somewhat secondary to excitatory processes, as coming along to keep excitation in check, to 'neaten up' the patterns of neural activity.

III. The fundamental role of inhibition in the brain. In fact, inhibition has a much more profound function in the brain than to act  merely as a check for excitation.  The exact role for inhibition seems somewhat different on the sensory side compared with the motor side of things, but inhibition's role is actually the same in both the sensory and motor spheres.  During preconscious motor planning, inhibition's role is to actively suppress the excitation of neurons during the period of time when prehensive networks for potential movements are being formed.  This role of inhibition will be further described for the motor system.  On the sensory side of things, inhibition stabilizes the neurons of the system so that new potential prehensive networks, any one of which would, when active, bring to awareness a new act of perceptual knowing, can be formed. During preconscious processing, when inhibition rules, potential prehensive neural networks are systematically elaborated. When the assent to act changes to an intent to act, a potential neural network - the brain's best guess as to a means to accomplish the goal of the action - explodes into electrochemical activity, conscious awareness blossoms, and we act.
Consider the dorsal column - medial lemniscal (DC-ML) component of the somatic sensory system, some connections of which are illustrated in the figure below.


     As with most other sensory systems, the nuclei of the DC-ML system that are considered in CNT to "relay" the encoded sensory information to higher centers for processing into representations and perceptions are richly innervated by fibers (shown in red & numbered 1, 2, 3) from the higher levels of the system. In fact, the number of corticothalamic fibers to the VPL thalamic nuclei from SI cortex is greater than the number of thalamocortical axons to SI cortex, a fact that clearly suggests the importance of such connections.  Another factor that suggests the importance of such connections is the persistence of such connections, via corticospinal fibers, to the dorsal horn (DH) of the spinal cord.  The space available for axonal traffic in the vertebral canal is limited and the fact that these connections are persistently present in the vertebrate brain is another pointer towards their having an important role.  While it is true that these fibers often engage (i.e., excite) local, inhibitory interneurons in the nuclei they innervate, they also sometimes cause excitation of the neurons that send their axons to the next level.
     What is the function of this fairly massive, "vertical" system of fibers that is found for all the general and special sensory systems?  Gerald Edelman <1> has proposed that activity of such "re-entrant" fibers is important in the generation of conscious awareness.  He emphasizes what might be called "horizontal" recurrent interconnections between higher levels of the system, for example between posterior parietal lobe and SII or regions of the extrastriate cortex which have brought in visual information.  We shall focus here on the "vertical" recurrent connections described above.

IV. The world as an "external memory."  One confusing problem to be dispensed with before attempting to put this all together is the idea that we are continually and rapidly processing sensory inputs to continuously update our internal model of the world.  Nothing could be further from the truth.  Neuronal signaling is far too low a bandwidth to allow any such activity.  Much of what we become aware of in an experiential event is, in fact, a memory of the world (see <2>), but one which, fortunately, rather exactly matches the actual world and which in not "within" the brain. This is a cardinal feature of the process philosophical approach and will not be discussed again at this time. (See material on the visual system.)  The point is that we are the world as previously sensed and objectively present, as we, on the verge of the conscious phase of a new experiential event, are attending to it with a point of view towards acting in it or on it in some way.  According to ecological neuroscience, perception is memory plus selection linked to intended action.

V. The bottom line. Well, if one can possibly make any sense out of this, it means that one important feature our sensory systems is that they are designed to exclude sensory information.  They are aided in this role by the descending, recurrent connections from 'higher' to 'lower' levels of the afferent pathways, such as were described for the DC-ML system above.  By maintaining activation of inhibitory interneurons (mostly), the sensory system is prevented from registering just any old stimulus.  In short, what we see or feel will not simply be what is there, but rather will be what we need to see or touch in order to take action on the world.  This point of view coincides with the recent findings of relative blindness to unexpected changes in the visual field (see <3>).  It requires that the neurons of our so-called "sensory pathways" be held under inhibitory control as some of them are incorporated into nonsensory prehensive neural networks tuned to affordances.  On this view, the organism actively selects, albeit preconsciously, the to-be-known-objects (TBKOs) on the basis of their affordances, i.e., on the opportunities for action that they afford the organism. The TBKOs are incorporated into potential prehensive neural networks, which include the object, the knower, and a nonsensory act of knowing while the neurons are inhibited.  Each new sensation is, at least to some very slight degree, a consequence of a decision or mood of intended action.  What does not afford an opportunity for action is not, or is only slowly, incorporated into a prehensive neural network, potential or real. This network, when activated by the object entering the receptive fields of the neurons that constitute it, will tend to fire synchronously, and at that point the act of knowing becomes perceptual, i.e., conscious, and we have entered into the mental pole of the experiential event.  We shall discuss in more detail the pivotal role of the motor system for perception later.  Here the focus has been on the fundamental role of inhibition during preconscious processing in the somatic sensory system.  According to this ecological neuroscience point of view, without inhibition we would be overwhelmed by input, assaulted by inappropriate sensory memories, and hopelessly lost to action.

VI. References and Notes

1. Edelman, G.M. Bright Air, Brilliant Fire: On the Matter of the Mind, NY: Basic Books, 1992.

2. O'Regan, J.K. The world as an 'external memory,' Can. J. Psychol. 46, 461-488, 1992.

3. O'Regan, J.K., Rensink, R.A., and Clark, J.J. Change-blindness as a result of 'mudsplashes,' Nature, 398: 34, 1999.