At an early stage of processing, a stimulus is represented as a set of contours. In the representation of form, a critical feature of these local contours is their orientation. In the present study, we investigate the representation of orientation at the somatosensory periphery and in primary somatosensory cortex. We record the responses of mechanoreceptive afferents and of neurons in areas 3b and 1 to oriented bars and edges using a variety of stimulus conditions. We find that orientation is not explicitly represented in the responses of single afferents, but a large proportion of orientation detectors (ϳ50%) can be found in areas 3b and 1. Many neurons in both areas exhibit orientation tuning that is preserved across modes of stimulus presentation (scanned vs indented) and is relatively insensitive to other stimulus parameters, such as amplitude and speed, and to the nature of the stimulus, bar or edge. Orientation-selective neurons tend to be more SA (slowly adapting)-like than RA (rapidly adapting)-like, and the strength of the orientation signal is strongest during the sustained portion of the response to a statically indented bar. The most orientation-selective neurons in SI are comparable in sensitivity with that measured in humans. Finally, responses of SI neurons to bars and edges can be modeled with a high degree of accuracy using Gaussian or Gabor filters. The similarity in the representations of orientation in the visual and somatosensory systems suggests that analogous neural mechanisms mediate early visual and tactile form processing.

At the somatosensory periphery, slowly adapting type 1 (SA1) and rapidly adapting (RA) afferents respond very differently to step indentations: SA1 afferents respond throughout the entire stimulus interval (sustained response), whereas RA afferents respond only at stimulus onset (on response) and offset (off response). We recorded the responses of cortical neurons to step indentations and found many neurons in areas 3b and 1 to exhibit properties that are intermediate between these two extremes: These neurons responded during the sustained portion of the stimulus and also at the offset of the stimulus. Several lines of evidence indicate that these neurons, which exist in large proportions even at these early stages of somatosensory cortical processing, receive input from both populations of afferents. First, we show that many cortical neurons have both a significant sustained response and a significant off response. Second, the strength of the off response is uncorrelated with that of the sustained response, which is to be expected if sustained and off responses stem from different populations of afferent fibers. Third, the bulk of the variance in cortical responses to step indentations can be accounted for using a linear combination of both SA1 and RA responses. Finally, we show that the off response in cortical neurons does not reflect rebound from inhibition. We conclude that the convergence of modality specific input onto individual neurons is common in primary somatosensory cortex and discuss how this conclusion might be reconciled with previous findings.

Neurons in area 3b have been previously characterized using linear spatial receptive fields with spatially separated excitatory and inhibitory regions. Here, we expand on this work by examining the relationship between excitation and inhibition along both spatial and temporal dimensions and comparing these properties across anatomical areas. To that end, we characterized the spatiotemporal receptive fields (STRFs) of 32 slowly adapting type 1 (SA1) and 21 rapidly adapting peripheral afferents and of 138 neurons in cortical areas 3b and 1 using identical random probe stimuli. STRFs of peripheral afferents consist of a rapidly appearing excitatory region followed by an in-field (replacing) inhibitory region. STRFs of SA1 afferents also exhibit flanking (surround) inhibition that can be attributed to skin mechanics. Cortical STRFs had longer time courses and greater inhibition compared with peripheral afferent STRFs, with less replacing inhibition in area 1 neurons compared with area 3b neurons. The greater inhibition observed in cortical STRFs point to the existence of underlying intracortical mechanisms. In addition, the shapes of excitatory and inhibitory lobes of both peripheral and cortical STRFs remained mostly stable over time, suggesting that their feature selectivity remains constant throughout the time course of the neural response. Finally, the gradual increase in the proportion of surround inhibition from the periphery to area 3b to area 1, and the concomitant decrease in response linearity of these neurons indicate the emergence of increasingly feature-specific response properties along the somatosensory pathway.

Studies of the visual system suggest that, at an early stage of form processing, a stimulus is represented as a set of contours and that a critical feature of these local contours is their orientation. Here, we characterize the ability of human observers to identify or discriminate the orientation of bars and edges presented to the distal fingerpad. The experiments were performed using a 400-probe stimulator that allowed us to flexibly deliver stimuli across a wide range of conditions. Orientation thresholds, approximately 20 degrees on average, varied only slightly across modes of stimulus presentation (scanned or indented), stimulus amplitudes, scanning speeds, and different stimulus types (bars or edges). The tactile orientation acuity was found to be poorer than its visual counterpart for stimuli of similar aspect ratio, contrast, and size. This result stands in contrast to the equivalent spatial acuity of the two systems (at the limit set by peripheral innervation density) and to the results of studies of tactile and visual letter recognition, which show that the two modalities yield comparable performance when stimuli are scaled appropriately.