Factors influencing cutaneous directional sensitivity: A correlative psychophysical and neurophysiological investigation

Abstract

The effects of 4 parameters of moving tactile stimuli (i.e., velocity, traverse length, position and orientation) on human cutaneous directional sensitivity and on the behavior of directionally sensitive neurons in S-I of unanesthetized macaque monkeys are studied. The experimental paradigms and approaches to data analysis are based on sensory decision theory (SDT), and provide indices of single neuron and of perceptual cutaneous direction sensitivity that can be compared. Human cutaneous directional sensitivity is shown to be maximal when the stimuli move at velocities between 5 and 30 cm/s, and to fall off either at lower or higher velocities. The neurophysiological studies of the effects of velocity reveal a heterogeneity in the population of directionally sensitive S-I neurons. Some neurons are shown to exhibit maximal directional sensitivity at velocities between 5 and 30 cm/s, whereas others possess maximal directional sensitivity at lower velocities (i.e., less than 5 cm/s). Human cutaneous directional sensitivity is determined at each of 5 different forelimb regions. The data reveal that a pronounced gradient in human cutaneous directional sensitivity exists along the proximodistal axis of the forelimb, with the greatest sensitivity existing at the most distal forelimb site studied. The companion neurophysiological studies reveal that a change in the position of the moving stimulus within the receptive field of an individual directionally sensitive S-I neuron is usually accompanied by a change in the magnitude of its directional sensitivity. Two major classes of directionally sensitive S-I neurons can be distinguished on the basis of the in-field variations in directional sensitivity they exhibit. For one neuron class, preferred direction remains the same at all regions within the receptive field; these are termed ‘direction invariant neurons’ and they appear to be capable of signalling direction of motion unambiguously under most of the experimental conditions used in this study. For the neurons of the second class, preferred direction varies with the position of the stimulus within the receptive field; these are termed ‘direction variant’ neurons. Direction variant S-I neurons signal movement toward or away from a given point within the receptive field. As a consequence, a reversal in cutaneous directional sensitivity within their receptive fields can typically be demonstrated. For every direction variant neuron studied the receptive field position at which cutaneous directional sensitivity reversed was located over a joint. The in-field organization of sensitivity demonstrated for direction variant S-I neurons prevents them from signalling direction of cutaneous motion in an unambiguous manner under many of the experimental conditions used in the present study. Human cutaneous directional sensitivity is demonstrated to increase progressively as the length of skin traversed by the moving stimuli is increased. Analysis of the neurophysiological data show that the two types of directionally sensitive S-I neurons identified in the studies of the effects of stimulus position can also be distinguished by the manner in which their directional sensitivity is altered by changes in stimulus traverse length. The ‘direction invariant’ S-I neurons exhibit a monotonically increasing relationship between traverse length and magnitude of directional sensitivity, while the direction variant S-I neurons do not. Human cutaneous directional sensitivity on the thenar eminence is for most subjects independent of the orientation of the moving tactile stimulus. In contrast, the neurophysiological data show that the directional sensitivity of both the direction invariant and the direction variant S-I neurons is orientation dependent: both classes of S-I neurons exhibit maximal directionality over a relatively restricted (usually less than 90°) range of stimulus orientations. Recognition that the positional relations between different sectors of a receptive field (especially those overlying joints) are modified by changes in body position leads to a hypothetical scheme for the processing of information about stimulus direction in the S-I cortex. This scheme requires the participation of both the direction invariant and direction variant S-I neuron populations identified in the present study.