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B-Afferents: a Fundamental Division of the Nervous System Mediating Hoxneostasis? Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 1990 Dichotomic classification of sensory neurons: Elegant but problematic Neuhuber, W L DOI: https://doi.org/10.1017/s0140525x00078882 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-154322 Journal Article Published Version Originally published at: Neuhuber, W L (1990). Dichotomic classification of sensory neurons: Elegant but problematic. Behav- ioral and Brain Sciences, 13(02):313-314. DOI: https://doi.org/10.1017/s0140525x00078882 BEHAVIORAL AND BRAIN SCIENCES (1990) 13, 289-331 Printed in the United States of America B-Afferents: A fundamental division of the nervous system mediating hoxneostasis? James C. Prechtl* Terry L* Powley Laboratory of Regulatory Psychobiology, Department of Psychological Sciences, Purdue University, West Lafayette, IN 47907 Electronic mail: [email protected]@brazil.psych.edu *Reprint requests should be addressed to: James C. Prechtl, Department of Neuroscience, A-001, University of California, San Diego, La Jolla, CA 92093 Abstract? The peripheral nervous system (PNS) has classically been separated into a somatic division composed of both afferent and efferent pathways and an autonomic division containing only efferents. J. N. Langley, who codified this asymmetrical plan at the beginning of the twentieth century, considered different afferents, including visceral ones, as candidates for inclusion in his concept of the "autonomic nervous system" (ANS), but he finally excluded all candidates for lack of any distinguishing histological markers. Langley's classification has been enormously influential in shaping modern ideas about both the structure and the function of the PNS. We survey recent information about the PNS and argue that many of the sensory neurons designated as "visceral" and "somatic" are in fact part of a histologically distinct group of afferents concerned primarily autonomic function. These afferents have traditionally been known as "small dark" neurons or B-neurons. In this target article we outline an association between autonomic and B-neurons based on ontogeny, cell phenotype, and functional relations, grouping them together as part of a common reflex system involved in homeostasis. This more parsimonious classification of the PNS, made possible by the identification of a group of afferents associated primarily with the ANS, avoids a number of confusions produced by the classical orientation. It may also have practical implications for an understanding of nociception, homeostatic reflexes, and the evolution of the nervous system. Keywords; autonomic; capsaicin; dorsal root ganglion; nerve growth actor; neuroimmunology; nociception; sensory neurons; substance P; sympathetics; tachykinins; visceral afferents 1. introduction which are incapable of directly giving rise to sensation." He was reluctant to classify afferents according to func- All of neuroscience uses the fundamental classification tional criteria, however, and hoped to rely eventually on that distinguishes the central and peripheral nervous morphological criteria. At the end of his 1903 paper he systems - the CNS and PNS, respectively - and classifies wrote: "Further progress awaits the discovery of some the elements of the PNS into subdivisions on the basis of distinguishing histological character [i.e., marker of auto- three dichotomies: afferent and efferent, skeletal and nomic afferents]." autonomic, and somatic and visceral. Given the paradig- Eighteen years later, in his book, The Autonomic matic importance of such a taxonomy, it is noteworthy Nervous System, Part I (1921), Langley excluded once that neither this accepted systematics nor the resulting and for all the possibility of autonomic afferents (see assignments have been rigorously reconsidered since the Figure 1). Although he planned (Langley 1921, p. 9) to beginning of the twentieth century, when they were reexamine this conclusion in a later publication, the considered tentative. In this target article, we suggest sequel to his 1921 work never appeared, and his "effer- that the categorization of PNS afferents, including a ents only" version of the ANS has been a source of description of their relation to the autonomic nervous continuing controversy. system (ANS), should be revised to reflect new informa- A number of neuroscientists, including authors of ma- tion about morphology, histochemistry, ontogeny, and jor treatises on the ANS (Gabella 1976; Mitchell 1953; function. Pick 1970), have expressed dissatisfaction with the As J. N. Langley developed his autonomic nervous "efferents only" concept. Nevertheless, it is commonly system concept, he carefully considered the possibility accepted in textbooks and in the general literature. Even that there was a specific class of afferents that also be- grant proposals have been criticized for suggesting that longed to this division of the nervous system. In 1903, specific afferents are associated with the ANS (see Nor- after having reviewed a number of possible criteria for gren 1985). Recently, some investigators have broken classifying afferents, Langley (1903, p. 25) tentatively with tradition and used terms such as "sympathetic af- concluded that autonomic afferents were those fibers ferents" (Foreman et al. 1986; Malliani 1982; Malliani et "which give rise to reflexes in autonomic tissues, and al. 1973; Morgan et al. 1986) and "parasympathetic af- © 1990 Cambridge University Press 0140-525X190 $5.00+.00 289 Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 10:57:47, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X00078882 Prechtl & Powley: B-Afferents Langley's PNS Concept (1921) (histochemically or pharmacologically) have charac- teristics that seriously challenge the validity of current Nerves classification systems. For example, substance P-contain- ing afferents, a subpopulation of B-neurons (section 3), not only mediate autonomic functions but have key on- togenetic and phenotypic traits similar to those of auto- (Dromic and Anti- Sympathetic Parasympathetic dromic action) nomic motor neurons. Nevertheless, according to Lan- (Plexuses of Auerbach and Meissner) gley's classification (Figure 1), these neurons would be, and indeed traditionally have been, lumped together Bulbo-sacral with all other spinal afferents. Alternatively, they are (oro>-anaI •*) fragmented into "general somatic" and "general visceral" categories by the doctrine of nerve components (Herrick r 1903; 1927). In this target article we analyze the inadequacies of the Figure 1. Langley's (1921, p. 10) classification of the pe- current classification systems and propose an alternative, ripheral nervous system. Note that all afferents are classified as "somatic," including those with antidromic actions. more parsimonious ordering. Our two main hypotheses are: (1) B-neurons represent a major division of the PNS, more fundamental than the traditional categories of "vis- ferents" (Kawatani et al. 1985; Mei 1985). Such desig- ceral" and "somatic." (2) The ANS is the motor system nators have important uses and in some cases have satis- most closely related to the B-neuron division. In one fied specific needs of specialists. It is uncertain whether sense, the B-neurons characterized here represent the they are sufficiently cogent to gain general acceptance, afferent division that Langley had searched for, but provi- however (see section 2.3). To date at least, none of these sionally ruled out. terms has stimulated a reformulation in the general literature. A common justification for such designators has been 2. Classification of nerwes and neurons that the afferents in question are found in the nerves, which are labeled "sympathetic" or "parasympathetic." The current terminology and concepts can be put in Langley was aware of the existence of afferents in auto- perspective by identifying their roots in some of the more nomic nerves but he did not regard this as a sufficient influential contributions to PNS classification and to the reason for invoking another autonomic neuron category. idea of homeostasis. He did not consider the ANS concept an invention for The distinctiveness of visceral function must first have heuristic convenience, but rather a discovery that could been recognized when these inner parts were found to be objectively repeated. Earlier, Gaskell (1886, p. 2) had move of their own accord, usually without the knowledge asserted that the test of a "real" fundamental division of of their owner. In the seventeenth century, such observa- the nervous system was whether the proposed functional tions led to the idea of involuntary nervous function, differences were "bound up with morphological dif- introduced to the study of functional anatomy by Thomas ferences." This approach had enabled Gaskell (1886) to Willis (Sheehan 1936). According to Willis (1664, 1965), delineate the bulbar, thoracolumbar, and sacral visceral the cerebrum mediated volition via the flow of animal nervous outflows and to achieve a revolutionary sim- spirits through the spinal cord and the cerebellum medi- plification of the nineteenth-century neuroanatomy. The ated involuntary functions through the vagal and inter- morphological difference that Gaskell used was the con- costal (sympathetic chain) nerves. The cerebrospinal sys- spicuously
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