Neural encoding of shape: Responses of cutaneous mechanoreceptors to a wavy
surface stroked across the monkey fingerpad.
LaMotte, Robert H. and Mandayam A. Srinivasan.
Department of Anesthesiology and Section of Neurobiology, 333 Cedar Street,
Yale University School of Medicine, New Haven, CT 06510, USA and Research
Laboratory of Electronics and Department of Mechanical Engineering,
Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
APStracts 3:0172N, 1996.
SUMMARY AND CONCLUSIONS
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 and rapidly-adapting type I mechanoreceptive afferents (SAs
and 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, while 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.
Received 5 September 1996; accepted in final form 15 August 1996.
APS Manuscript Number J586-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 29 August 1996