Surround suppression in the responses of primate SA1 and RA mechanoreceptive afferents mapped with a probe array.

Abstract

Twenty-four slowly adapting type 1 (SA1) and 26 rapidly adapting (RA) cutaneous mechanoreceptive afferents in the rhesus monkey were studied with an array of independently controlled, punctate probes that covered an entire fingerpad. Each afferent had a receptive field (RF) on a single fingerpad and was studied at 73 skin sites (50 mm2). The entire array was lowered to 1.6 to 3.0 mm below the point of initial skin contact (the background indentation) before delivering indentations with one to seven probes. Indentations were generally limited to 100 microm to minimize gross mechanical interactions. There were two major, new findings. 1) The discharge rates of both SA1 and RA afferents were strongly affected by the number of probes indenting the RF simultaneously. The effect was exponential. Each increase in probe number reduced the response by 24% in SA1 and 12% in RA afferents on average. When seven probes indented the skin simultaneously, the impulse rates in SA1 and RA afferents were reduced to 20 and 40% of the rates evoked by a single probe at the hot spot (all indentations were 100 microm). This shows that before any synaptic interaction in the CNS there is already a mechanism analogous to surround inhibition that suppresses an afferent's responses to uniform indentation and makes it especially sensitive to deviations from spatial uniformity. 2) The responses of both SA1 and RA afferents were independent of background array depth over the range from 1.6 to 3 mm below the point of initial skin contact. This shows that the neural responses to elements raised above a background are independent of the applied force over a wide range of forces. To relate the background depths to indentation force and to compare humans and monkeys, we studied the biomechanics of indentation with a uniform surface. A remarkable result is that the force-displacement relationships in humans and monkeys were the same; the skin is highly compliant for the first 2-3 mm of indentation and then becomes much stiffer. The results were the same in alert humans and monkeys and in monkeys anesthetized with pentobarbital. Ketamine anesthesia made the skin much stiffer and reduced the compliant range substantially.