Neural coding of tactile texture: comparison of spatial and temporal mechanisms for roughness perception

Abstract

A previous study showed that roughness perception may depend on either temporal or spatial variations in firing rate among cutaneous mechanoreceptive afferents. The present study was designed to distinguish between these hypotheses. Plastic surfaces embossed with patterns of dots designed to produce predictable alterations in temporal and spatial firing rate variation were used as stimuli in psychophysical and neurophysiological experiments. Subjective roughness magnitudes obtained from psychophysical experiments fitted the predictions of the spatial but not the temporal hypothesis. In the neurophysiological experiments, the stimuli were scanned across the receptive fields of cutaneous mechanoreceptive afferents. Firing rate variation in the neural responses was measured using a range of temporal and spatial filters. Temporal variation was not correlated with roughness magnitude. Spatial variation, on a scale of 1-2 mm (one to two receptor spacings), was closely correlated with roughness.

Evidence for the duplex theory of tactile texture perception

“…The most likely explanation, however, is that their gratings, being spatially periodic, gave rise during movement but not during static touch to mechanoreceptor activity characterized by strong temporal periodicities (Darian-Smith & Oke, 1980). Although temporal cues do not appear to contribute to the roughness of coarse textures in a scaling task (Connor et aI., 1990;Connor & Johnson, 1992), they might be utilized in a discrimination task if spatial information were marginal. Because of the haphazard arrangement of particles on abrasive surfaces, temporal periodicity was not a factor in the present study, perhaps resulting in a crisper transition between spatial and nonspatial mechanisms of texture perception.…”

“…A series of studies by Johnson and colleagues (summarized by Johnson & Hsiao, 1992) has made it clear that perception of such properties (e.g., identification ofraised letters) depends largely on the processing of signals from slowly adapting Type I (SA I) mechanoreceptors; from primary afferents (Phillips, Johansson, & Johnson, 1990) to cortical neurons (Phillips, Johnson, & Hsiao, 1988), this mechanoreceptive system demonstrates a remarkable ability to register and extract information about the spatial arrangement offeatures that are large enough to be individually discerned. Moreover, Connor, Hsiao, Phillips, and Johnson (1990;Connor & Johnson, 1992) have shown explicitly that people use this system to judge the roughness of coarse surfaces and that their judgments reflect computations, apparently made in somatosensory cortex, using spatial algorithms.…”

“…For example, another early study (Meenes & Zigler, 1923) reported that subjects who described moving textured stimuli as rough or smooth did not find these terms appropriate to describe the same surfaces when lateral movement was disallowed, preferring to describe their sensations in terms of even or uneven pressure; but there is no indication in their study that this was more true of fine textures than of coarse textures. More recent studies of roughness perception generally confine themselves to relatively coarse textures (Connor et aI., 1990;Connor & Johnson, 1992) or do not measure performance under conditions of static touch (Heller, 1989;Lamb, 1983;Lederman, 1974;Lederman & Taylor, 1972;Stevens & Harris, 1962;Taylor & Lederman, 1975). Thus, Phillips, Johnson, and Browne's (1983, p. 243) prediction that "texture discrimination ... that is believed to depend on information relayed by the [vibration-sensitive] rapidly adapting afferents should be profoundly affected by skin movement" has rarely been subjected to quantitative test.…”

A dense array stimulator to generate arbitrary spatio-temporal tactile stimuli

“…The rotating drum has been used to scan various types of raised patterns across the glabrous skin of both monkeys (Connor et al, 1990;Connor and Johnson, 1992;Blake et al, 1997;DiCarlo et al, 1998;DiCarlo and Johnson, 1999Yoshioka et al, 2001), in neurophysiological experiments, and humans in psychophysical and percutaneous recording experiments (Phillips et al, 1992). Stimuli such as raised letters and textured surfaces are mounted on a drum; the drum is brought in contact with the skin and rotated.…”

“…By moving the drum in small increments laterally, a spatial pattern can be moved across the fingerpad while single-unit recordings are made. Recordings of both peripheral (Connor et al, 1990;Connor and Johnson, 1992;Blake et al, 1997;Yoshioka et al, 2001) and central DiCarlo et al, 1998;Johnson, 1999, 2002) neurons have been made with this device. The same spatial patterns can be presented to human observers in psychophysical tasks in which they are asked to identify the patterns.…”