ArticlesPatterns in the brain: Neuronal population coding in the somatosensory system
Introduction
The sense of touch constitutes the interface between the external world of objects and our internal world of self. It is both an active sense for exploring and manipulating the environment, and a passive sense for receiving touch that can stir the emotions as well as inform. Unlike other senses, touch is simultaneously given and received by simple mutual contact of the skin. It is a young girl caressing her silken, gray cat, a carpenter feeling the grain of his newly carved table, a physician palpating a sensitive abdomen, a lover's touch that leads to a kiss, a blind man fingering a pattern of raised dots in order to “see.”
How does this sense of touch come about? What are the neural mechanisms responsible for the rich variety of somatosensory experiences? As G. E. Smith [107] observed “… all the kaleidoscopic manifestations of mental activity are dependent upon, and determined by, physiological processes taking place in the nervous system.” But what is the nature of those processes, especially as they apply to somesthesis? The aim of this review is to address those questions, based primarily on the author's own research in sensory processing and on related neural coding studies by others. The review concentrates on stimulus coding by populations (ensembles) of neurons and is limited mainly to discussion of the somatosensory system.
The history of neural coding is marked by a pervasive tension between two seemingly contradictory ideas—that different sensory functions are mediated by activation of distinctly different neurons with highly specific stimulus sensitivities, or that different functions are represented by unique patterns of activity in populations of neurons with relatively broad stimulus sensitivities. The “specificity” theory had its origins in Johannes Müller's doctrine of “specific nerve energies” [79], which emphasized the unique functional characteristics of the nerves mediating different sense modalities. That doctrine was subsequently extended by von Helmholtz [48] and von Frey [39] to become the principle of “specific fiber energies,” which held that each stimulus submodality or quality within a sense modality is encoded by excitation of different specific nerve fibers or neurons. The modern version of this theory is often referred to as the “labeled-line” code. Support for this view was driven largely by new electrophysiological techniques that made it possible to determine the physiological properties, response characteristics, and receptive fields of individual neurons. The predominance of the specificity idea is exemplified by the ubiquitous phrase, “place- and modality-specific neurons,” in the neuroscience literature. This notion is also reflected in various proposals for different classes of cells signaling “touch, vibration, pain, cold, position, movement, etc.” in somesthesis, “red, green, edge, orientation, direction of movement, etc.” in vision, and “salty, sweet, sour, etc.” in gustation. With its emphasis on individual cells, the labeled-line notion has been explicitly or implicitly advocated by many investigators 4, 19, 38, 52, 64, 66, 76, 78, 90, 93, 94, 95.
In contrast, the “pattern” theory had its origins in the theory of color vision proposed by Thomas Young [124] and elaborated by von Helmholtz [49]. The theory stated that the retina contains three different receptors that are broadly, but differentially, sensitive to all portions of the spectrum—any wavelength of light (color) can thus be uniquely represented by the ratios of responses across the different types of receptors. This basic idea was adopted in varying form or developed independently by others including Adrian et al. [3], Pfaffmann 91, 92, Weddell [118], Erickson 25, 26, Towe [111], Mountcastle 76, 78, Doetsch and Erickson [14], John [56], Doetsch and Towe [15], Whitfield [120], Ray and Doetsch [99], and Nicolelis et al. 82, 83. In the modern period, Pfaffmann [92] was the first to make a formal statement of the pattern theory in his description of gustatory coding; surprisingly, he later adopted a position more consistent with the labeled-line theory [93]. However, it was Robert Erickson [25] who put the matter most succinctly: “… the neural message for gustatory quality is a pattern made up of the amount of neural activity across many neural elements.” Erickson 23, 24, 26, 27 then proceeded to develop this notion into a comprehensive theory, and extended its application to all sensory, motor, and cognitive systems of the brain, suggesting that “across-neuron response patterns” constitute the fundamental language of the nervous system. The basic difference between the two theories is illustrated schematically in Fig. 1.
Some versions of the pattern theory tended to neglect the role of specialized receptors and neurons, suggesting that different patterns of excitation in space and time were the sole determinants of different sensory experiences 80, 118. This view was later modified to include the role of differentially sensitive receptors and central neurons 70, 106. In contrast, the original Young–Helmholtz theory did not have this problem, because it explicitly required different types of retinal receptors. Likewise, the pattern theory developed by Erickson 23, 24, 25, 26, 27 demands the existence of differentially tuned neural elements at all levels of the nervous system, from receptors to cerebral cortex. Furthermore, the theory incorporates the idea of specificity in terms of anatomically and functionally distinct systems mediating different sensory, motor, and cognitive processes. Hence, neural specificity, within certain broad limits, and population coding are not mutually exclusive. A peripheral nerve, nucleus, or brain area is developmentally specified to perform or contribute to certain functions (such as somatosensory or visual perception)—but precise coding of information within that anatomical/functional entity is accomplished by patterns of activity across neuronal populations that are unique for each sensory-perceptual experience (see [89] for a catalogue of candidate neural codes).
Section snippets
Theory of coding by across-neuron response patterns
The central principle of the across-neuron response pattern (ANRP) theory, sometimes referred to as the “across-fiber pattern” theory 23, 24, 25, 26, 27, is that information is encoded by neuronal populations and not by individual neurons. More specifically, precise information is represented in the nervous system by spatiotemporal patterns of activity and amounts of activity in ensembles of nerve fibers and central neurons. The basis for this proposition is that the sensitivity functions or
Developmental specification of function: Cerebral cortex and its inputs
How is cortical function initially specified in brain development, and how does this relate to the problem of neural coding? During the early cell migration phase of development, the neocortex is not segregated into unique sensory and motor areas, but appears to consist of a functionally homogeneous or equipotential “protocortex” [86]. A “proto-map” of prospective cortical areas may be present in the germinal epithelium, so that the final tangential location of a cortical neuron is determined
Acknowledgements
I thank Douglas D. Rasmusson, Richard H. Ray, and S. David Stoney, Jr. for very helpful comments on this manuscript. I am especially grateful to Robert P. Erickson for many stimulating discussions over the years, for his continued support of my work, and for his enduring friendship.
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