Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey

Abstract

This is the second in a series of studies of the neural representation of tactile spatial form in cortical area 3b of the alert monkey. We previously studied the spatial structure of 330 area 3b neuronal receptive fields (RFs) on the fingerpad with random dot patterns scanned at one velocity (40 mm/sec; DiCarlo et al., 1998). Here, we analyze the temporal structure of 84 neuronal RFs by studying their spatial structure at three scanning velocities (20, 40, and 80 mm/sec). As in the previous study, most RFs contained a single, central, excitatory region and one or more surrounding or flanking inhibitory regions. The mean time delay between skin stimulation and its excitatory effect was 15.5 msec. Except for differences in mean rate, each neuron's response and the spatial structure of its RF were essentially unaffected by scanning velocity. This is the expected outcome when excitatory and inhibitory effects are brief and synchronous. However, that interpretation is consistent neither with the reported timing of excitation and inhibition in somatosensory cortex nor with the third study in this series, which investigates the effect of scanning direction and shows that one component of inhibition lags behind excitation. We reconcile these observations by showing that overlapping (in-field) inhibition delayed relative to excitation can produce RF spatial structure that is unaffected by changes in scanning velocity. Regardless of the mechanisms, the velocity invariance of area 3b RF structure is consistent with the velocity invariance of tactile spatial perception (e.g., roughness estimation and form recognition). Key words: receptive field; somatosensory; cortex; area 3b; SI; tactile; velocity; monkey; reverse correlationThe study reported here concerns the temporal and spatial response properties of neurons in area 3b of primary somatosensory cortex. Previous studies of area 3b have shown that each point in a neuron's cutaneous receptive field (RF) may give rise to excitation, inhibition, or both (Mountcastle and Powell, 1959;Laskin and Spencer, 1979; Gardner and Costanzo, 1980b,c;DiCarlo et al., 1998), that there is a delay between the cutaneous stimulus and the response (Mountcastle and Powell, 1959;Laskin and Spencer, 1979;Gardner and Costanzo, 1980a), that the excitatory and inhibitory effects may persist for variable periods (Laskin and Spencer, 1979;Gardner and Costanzo, 1980b), and that the timing of excitation and inhibition arising from a single cutaneous site may be different (Laskin and Spencer, 1979;Gardner and Costanzo, 1980b). Thus, area 3b RFs have temporal, as well as spatial structure. Although the precise relationship between the spatial and temporal parameters of a neuron's response and the RF estimated with a scanned stimulus is complex (see Appendix A), the general effects of temporal delay between the stimulus and response are as follows. Because we do not initially know the delay between the stimulus and each response component, our RF estimation procedure assigns each response component to the...

Neuronal correlates of tactile speed in primary somatosensory cortex

“…C: subjective speed estimates showed a similar monotonic increase with speed, but speed estimates were lower for the rougher surface (data replotted from Dépeault et al 2008). surfaces, and simulated moving bars generated with multiprobe arrays (DiCarlo and Johnson 1999;Gardner et al 1992;Romo et al 1996;Tremblay et al 1996;Whitsel et al 1972). The absence of negative ("inhibitory") responses to speed in our sample compared with earlier studies (e.g., DiCarlo and Johnson 1999;Sinclair and Burton 1991) can be explained by the sampling procedure, since only neurons showing an increase in discharge during surface scanning were tested.…”

“…Consistent with this, a number of studies have shown that S1 cortical neurons are sensitive to tactile motion, using a variety of approaches including mechanical indentation of the skin (Esteky and Schwark 1994), sequential stimulation of a fixed length of skin (Gardner et al 1992;Pei et al 2010;Romo et al 1996;Whitsel et al 1972), and tangential scanning of surfaces over a fixed location on the skin with the subject either immobile, passive touch (DiCarlo and Johnson 1999;Sinclair et al 1996;Tremblay et al 1996) or moving, active touch (Sinclair and Burton 1991). The results indicate that sensitivity to the speed of tactile motion is present in all three areas that form the primate cutaneous hand representation, areas 3b, 1, and 2.…”

A dense array stimulator to generate arbitrary spatio-temporal tactile stimuli

“…The rotating drum has been used to scan various types of raised patterns across the glabrous skin of both monkeys (Connor et al, 1990;Connor and Johnson, 1992;Blake et al, 1997;DiCarlo et al, 1998;DiCarlo and Johnson, 1999Yoshioka et al, 2001), in neurophysiological experiments, and humans in psychophysical and percutaneous recording experiments (Phillips et al, 1992). Stimuli such as raised letters and textured surfaces are mounted on a drum; the drum is brought in contact with the skin and rotated.…”

White Noise Analysis of Coupled Linear-Nonlinear Systems

“…(Parameters needed are 1 = 2 = 0 so that δ 1 = δ 2 = 1, as well asr 1 =r 2 = 1, cosθ k pp = 1 for k = 0 and cosθ j pq = 0 for p = q.) 6 In this case, the matrixà could become almost singular, and its inversion would not be stable.…”

“…The most common use of white noise analysis has been to analyze the response properties of single neurons [11,4,5,8,9,2,3,16,18,7,6]. Recently, researchers have begun to apply the techniques of white noise analysis to simultaneous measurements of multiple neurons [15,1,19], although without explicitly modeling neural connectivity.…”