A distinctive feature of the parietal cortex is the presence of a species-specific diminutive form concerned with somatic sensory perception. The term “homunculus,” borrowed from Aristotelian preformationism, has been used to describe the disproportionate neural representation of the somatic sensory epithelium in the postcentral gyrus with respect to the body but proportionate to the actual innervation density in the periphery. Peripheral axons of dorsal root ganglion cells innervate a variety of sensory receptors located in differing densities along the body surface, and the trigeminal ganglion axons do the same for the orofacial regions. Central axons of these primary sensory neurons not only convey a variety of somatic sensory information ranging from touch, pressure, pain, thermo- and proprioception to the central nervous system, but they also form topographic maps of the body surfaces from which they carry information within dorsal column and brainstem trigeminal nuclei. These maps are then transferred, via the lemniscal pathways, to the ventroposterolateral and ventroposteromedial nuclei of the thalamus, and subsequently to the primary somatosensory cortex. Convergence and divergence of neural inputs along this trisynaptic pathway, coupled with the species-specific differential distribution and density of sensory receptors in the somatic periphery, present a caricature of a cortical body map that is an exaggeration of the most characteristic and striking features of a particular animal's somatic sensory world. In addition to the cortical parcellation that is devoted to the representation of the somatic body map, patterning within map components can be further visualized with routine histological stains. Whisker- and digit-specific barrels of the rodent or nasal appendage representations of the star-nose mole primary somatosensory cortex are some of the most prominent examples of body map organization. Experimental manipulations or genetic aberrations that alter sensory peripheral receptor sheets have taught us the malleability of central body maps and their plasticity. Other in vitro and in vivo studies have revealed the multifaceted complexity of mechanisms underlying the development of topographic sensory maps and patterning of neural connections within map subdivisions. The present consensus is that a variety of molecular cues and transcription factors play a major role in guiding sensory axons to their proper targets, forming topographic maps in subcortical and cortical terminal fields, and invoking neural activity-dependent mechanisms in order to help construct and refine patterns within the boundaries of somatosensory circuits.
In this special issue of The Anatomical Record, “Many Faces of Somatosensory Cortex: From Molecules to Maps,” we present a collection of research and review articles that highlight different facets of somatosensory map development and patterning in subcortical and cortical areas. The first article, by Erzurumlu et al., provides an extensive review on the role of neurotrophins, various axon guidance molecules, transcription factors, and glutamate receptors in the development of the rodent brainstem trigeminal nuclei, the first relay station of the CNS for facial mapping. Molecular and cellular mechanisms that set up the face map in the brainstem and lead to whisker-specific patterning within the map may also be operational at the thalamic and cortical levels. Uziel et al. discuss the role of Eph/ephrin family of molecules in the presorting of thalamocortical axons that convey somatosensory maps to the primary somatosensory cortex. These guidance molecules have been implied in the topography of connections between the sensory thalamus and the neocortex and reciprocal projections to the sensory thalamus. McIlvain and McCasland underscore the role of the axon guidance and neural plasticity molecule GAP-43 in thalamocortical targeting and radial glial differentiation. Despite delays in the development of these elements in GAP-43 heterozygous mice, they do not detect shifts in the timing of critical period plasticity following neonatal whisker lesions, suggesting that the plasticity window might be determined subcortically. Ferrere et al. describe expression of homeobox genes Cux-1 and Cux-2 during the development of the mouse barrel cortex and in barrel-defective mouse strains, such as the VMAT2, MAOA, and Adcyl type 1 knockout mice. They provide evidence that Cux-1 is a reliable marker of layer IV barrel neurons and that Cux-1 and Cux-2 are differentially regulated in a layer-specific manner in the developing somatosensory cortex.
Simpson et al. focus on noradrenergic projections from locus coeruleus to the barrel cortex. Using immunohistochemistry, they provide data indicating that noradrenergic projections to the barrel fields are not patterned, which is in contrast to the localized concentrations of serotonin seen within thalamocortical terminals during development. Waite et al. investigate whisker maps in marsupials, and the effects of lesions of the whisker afferent carrying component of the trigeminal nerve in wallaby, a species with a protracted development of trigeminal lemniscal pathways leading to the barrel cortex. Examination of critical period plasticity in this species reveals that there is a single critical period plasticity for the thalamus and cortex that coincides with maturation of cortical barrel patterns. Kaas et al. focus on a less explored area of the body map in primates, the representation of teeth and tongue. They report that parts of areas 3b, 3a, and 1 are involved in processing mechanoreceptor information flowing from the teeth and tongue and discuss these results in relation to gustatory information processing in the cortex.
“Homunculi,” “ratunculi,” body maps on either side of the brain talk to each other via callosal connections and also communicate with other primary sensory cortices via association cortex. The last two articles in this special issue present data on the development of callosal projections in humans (Richard group, Ren et al.) and point to common molecular mechanisms in the guidance of callosal axons between humans and mice. Finally, Crish et al. examine the visual pathways of a fossorial rodent species that has an extremely well-developed somatosensory system, spends most of its life in subterranean burrows, and has a degenerate eye and optic nerve. Curiously, this species has visual structures that are related to circadian rhythms but have “lost” primary visual processing pathways.
The collection of studies in this special issue is intended to present the reader with a compendium of brain mechanisms that govern the formation of central representation of the sensory periphery, i.e., maps with a particular emphasis on the “many faces” of the somatosensory cortex.