Abstract
Touch is encoded by cutaneous sensory neurons with diverse morphologies and physiological outputs. How neuronal architecture influences response properties is unknown. To elucidate the origin of firing patterns in branched mechanoreceptors, we combined neuroanatomy, electrophysiology and computation to analyze mouse slowly adapting type I (SAI) afferents. These vertebrate touch receptors, which innervate Merkel cells, encode shape and texture. SAI afferents displayed a high degree of variability in touch-evoked firing and peripheral anatomy. The functional consequence of differences in anatomical architecture was tested by constructing network models representing sequential steps of mechanosensory encoding: skin displacement at touch receptors, mechanotransduction and action-potential initiation. A systematic survey of arbor configurations predicted that the arrangement of mechanotransduction sites at heminodes is a key structural feature that accounts in part for an afferent's firing properties. These findings identify an anatomical correlate and plausible mechanism to explain the driver effect first described by Adrian and Zotterman. DOI: http://dx.doi.org/10.7554/eLife.01488.001.
Highlights
A diverse array of touch receptors allows animals to discern object shapes, to explore surface textures and to detect forces impinging upon the skin
We identified slowly adapting type I (SAI) afferents by their immunoreactivity to Neurofilament H (NFH; a myelinatedneuron marker) and by their contacts with Keratin-8-positive Merkel cells in touch domes, which are specialized skin regions that surround tylotrich hairs (Figure 1B,C)
We did not observe immunoreactivity against voltage-activated sodium or potassium channels in unmyelinated neurites juxtaposed to Merkel cells (N = 201 Merkel cell-neurite complexes), it is possible that these channels are present at levels below detection threshold
Summary
A diverse array of touch receptors allows animals to discern object shapes, to explore surface textures and to detect forces impinging upon the skin. Distinct classes of mechanosensory afferents are tuned to extract specific features of a tactile stimulus and to encode them as trains of action potentials, or spikes, with unique firing properties (Johnson, 2001). A common feature of mechanosensory neurons is specialized anatomical structures, termed end organs, that shape their neuronal outputs (Chalfie, 2009). Sensory stimuli act at peripheral terminals to produce receptor potentials, which locally sum to trigger spikes that travel to central terminals up to 1 m away. A landmark study of Pacinian corpuscles established that spikes initiate at the heminode, the most distal node of Ranvier (Loewenstein and Rathkamp, 1958). A Pacinian corpuscle is innervated by an un-branched afferent; most tactile end organs comprise branching afferents with multiple sites of sensory transduction
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