Population estimates for responses of cutaneous mechanoreceptors to a vertically indenting probe on the glabrous skin of monkeys

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Abstract
Recordings were obtained from low-threshold mechanoreceptive afferents during stimulation with a 0.5-mm-diameter probe at the receptive field (RF) center and at different distances from the point of maximal sensitivity. At each location, force-controlled stimuli of 0.5–4.0 g were ramped on to a plateau and then off at rates of 1, 10, and 100 g/s. The properties of rapidly adapting (RA) and slowly adapting type I (SAI) mechanoreceptors, when stimulated at the RF center, were similar in many respects to those reported in previous studies. Controlled stimulation away from the RF centers revealed that RF size for RAs was primarily dependent upon ramp rate, and for SAIs the size of the RF was primarily dependent upon load (force). The action potentials from individual afferents during stimulation at each location were binned in time and assigned to spatial segments of 1 mm. These responses were multiplied by: (A) an annular area of the receptive field and (B) the innervation density for the afferent type and skin region. The calculations provided estimates of overall rates of activity among the population of cutaneous afferents that respond to indentation by a small probe. Important differences were obtained between the responses of the population of afferents activated by the trapezoidal stimulus and the responses of afferents stimulated only at the RF center. Populations of tactile afferents provide more information for rate and intensity (force) discriminations than is available from units stimulated at the RF center. For RA afferents, the exponent of the power function describing relationships between stimulus rate and the population discharge (in impulses per second) was 0.3 times greater than the exponent for responses to on-center stimulation. For SAI mechanoreceptors, the exponent of the power functions for static responses to force was 0.22 times greater for the population responses than for on-center activation. Population functions for RA responses to the rate of force application and for SAI responses to static load saturated less than comparable responses to stimuation of the RF center. Thus, the coding capacity of the population extends the range of tactile discriminability. The slope and range of stimulus-response functions for populations was enhanced relative to responses to oncenter stimulation. This occurs because of recruitment of afferents with RF centers adjacent to and remote from the stimulus, depending upon thresholds and receptive field sizes for different stimulus parameters. With stimulation at increasing rates and forces, there is a progressive spatial recruitment of receptors. Over 90% of the activity elicited by suprathreshold punctate stimuli originated from mechanoreceptors with RF centers 1 mm or more away from the stimulus site. When the population response of SA afferents was calculated for different intensities of plateau stimulation, ranging from 1 to 4 g, the slope of the power function corresponded well to psychophysical estimates in the literature on the growth of touch intensity. Recruitment of afferents stimulated off the RF center shaped the temporal pattern of discharge. For RA afferents, the population response reached peak rates toward later portions of the onset and offset response than for on-center stimulation. For SAI afferents, the population discharge during slow onsets accelerated more positively than the responses to on-center stimulation. Variations in the rate, amplitude, and duration of stimulation were demonstrated to be useful in assessing the contribution of SAI and RA afferents to different tactile sensations. At very slow rates of stimulus application, the RA response was so minimal that the population response can be considered to arise from SAI afferents. At high stimulus rates, the population response was greatly accentuated during the onset (indentation) and offset (removal) of a trapezoidal ramp-and-hold stimulus, relative to firing rates during maintained indentation. Ratios of dynamic to static discharge were 3–4 times greater for the population than for on-center stimulation, reaching values as high as 60.2∶1. The ratios of dynamic to static population responses were greatest for stimuli presented to the palm and were least for stimuli presented to the base and middle phalanges of the fingers. Therefore, the relative magnitudes of onset, offset, and steadystate sensations elicited by stimulation at different rates and locations should vary systematically, according to the absolute and relative densities of each receptor type.