Neural encoding of shape: responses of cutaneous mechanoreceptors to a wavy surface stroked across the monkey fingerpad.
1. The role of cutaneous mechanoreceptors in the tactile perception of shape was investigated. Objects whose surfaces were shaped as a pattern of smooth, alternating convex and concave cylindrical surfaces of differing radii of curvature were constructed such that there were no discontinuities in the slope of the surface. These "wavy surfaces" were stroked across the fingerpad of the anesthetized monkey and electrophysiological responses of slowly adapting type I mechanoreceptive afferents (SAs) and rapidly adapting type I mechanoreceptive afferents (RAs) were recorded. 2. For both SAs and RAs, each convexity indenting the skin evoked a burst of impulses and each concavity of the same curvature that followed elicited a pause in response. "Spatial event plots" (SEPs) of the occurrence of action potentials as a function of the location of the object on the receptive field were obtained and interpreted as the responses of a spatially distributed population of fibers. With increasing magnitude of curvature (equivalently, decreasing radius of curvature) of convexity, the mean width of the burst in the SEPs for each fiber type (representing the width of a region of skin containing active fibers) decreased and the mean discharge rate during the burst increased. Over a range of velocities of stroking from 1 to 40 mm/s, the number of RAs activated increased with velocity, whereas SAs were active at all velocities. For both SAs and RAs, the burst rates increased with velocity, whereas the widths of the bursts and pauses remained approximately invariant. Thus the spatial measures of burst or pause width provide a robust representation of the size of a feature on the object surface. 3. For a given velocity of stroking, the spatially distributed pattern of averaged discharge rates (spatial rate profile, SRP) provided a representation of the shape of the wavy surface. The distance between neighboring peaks in the SRP for individual RAs and SAs was approximately the same as the distance between the peaks of the wavy surface. The averaged SRP for a population of SAs provided a better representation of shape than that for RAs. Whereas active regions in the SEP can be isomorphic to the two dimensional form of the stimulus "footprint" in contact with the skin surface, the SRP, which in addition encodes the features of the stimulus in the third dimension normal to the skin surface, is not isomorphic to the stimulus shape. 4. When the sizes as well as the shapes of objects are varied, it is hypothesized that a central processing mechanism extracts the invariant property of shape from the slopes of the rising and falling phases of an SRP that has been normalized for overall differences in discharge rates. These differences would be expected to occur with variations in the parameters of stimulation such as compressional force, stroke trajectory, and stroke velocity. It was shown that a common feature of the mean SRP for SAs evoked by each wavy surface convexity, regardless of its radius, was the constancy of the slope from the base to the peak and from the peak to the base. Thus a possible code for the constant curvature of a cylinder is the constancy of the slopes along the rising and declining phases of the triangular-shaped spatial response profile evoked in the SA population by the cylindrical convexity.
LaMotte
R H
RH
Department of Anesthesiology, Yale University School of Medicine, New Haven, Connecticut 06510, USA.
Srinivasan
M A
MA
D000818:Animals; D005071:Evoked Potentials / Q000502:physiology; D005385:Fingers / Q000294:innervation*; D005556:Form Perception / Q000502:physiology*; D008252:Macaca fascicularis; D008465:Mechanoreceptors / Q000502:physiology*; D010812:Physical Stimulation; D012867:Skin / Q000294:innervation*; D013499:Surface Properties; D009435:Synaptic Transmission / Q000502:physiology*; D014110:Touch / Q000502:physiology*; D014741:Video Recording