Precise and stable edge orientation signaling by human first-order tactile neurons

Abstract

Fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) first-order neurons in the human tactile system have distal axons that branch in the skin and form many transduction sites, yielding receptive fields with many highly sensitive zones or subfields. We previously demonstrated that this arrangement allows FA-1 and SA-1 neurons to signal the geometric features of touched objects, specifically the orientation of raised edges scanned with the fingertips. Here we show that such signaling operates for fine edge orientation differences (5-20{degrees}) and is stable across a broad range of scanning speeds (15-180 mm/s); that is, under conditions relevant for real-world hand use. We found that both FA-1 and SA-1 neurons weakly signal fine edge orientation differences via the intensity of their spiking responses and only when considering a single scanning speed. Both neuron types showed much stronger edge orientation signaling in the sequential structure of the evoked spike trains and FA-1 neurons performed better than SA-1 neurons. Represented in the spatial domain, the sequential structure was strikingly invariant across scanning speeds, especially those naturally used in tactile spatial discrimination tasks. This speed invariance suggests that neurons responses are structured via sequential stimulation of their subfields and thus links this capacity to their terminal organization in the skin. Indeed, the spatial precision of elicited action potentials rationally matched spatial acuity of subfield arrangements, which typically corresponds to the dimension of individual fingertip ridges. Significance StatementThe distal axons of human first-order tactile neurons branch and innervate many mechanosensitive end organs in the skin. For those neurons terminating in end organs associated with fingerprint ridges (Meissner and Merkel), this branching results in cutaneous receptive fields with multiple subfields spread across several ridges. Consequently, when a fingertip scans the surface of an object, the spatial coincidence between a neurons subfields and the tactile stimulus defines the sequential structure of the evoked spike train (i.e., the presence of action potential bursts and the gaps between them). Here we show that, for surfaces composed of oriented edges, this sequential structure signals information about edge orientation differences at the limit of what people can feel and that the spatial precision of the structuring is maintained across a broad range of speeds relevant for real-world hand use. We submit that, to be of human relevance, models of higher order tactile processing must consider the impact of multifocal receptive fields in the periphery. For example, the speed invariance of tactile fine-form/texture perception may arise simply because the same subsets of peripheral subfields in the population of first-order tactile neurons are stimulated together regardless of speed.