Spatiotemporal receptive fields of peripheral afferents and cortical area 3b and 1 neurons in the primate somatosensory system

Abstract

Neurons in area 3b have been previously characterized using linear spatial receptive fields with spatially separated excitatory and inhibitory regions. Here, we expand on this work by examining the relationship between excitation and inhibition along both spatial and temporal dimensions and comparing these properties across anatomical areas. To that end, we characterized the spatiotemporal receptive fields (STRFs) of 32 slowly adapting type 1 (SA1) and 21 rapidly adapting peripheral afferents and of 138 neurons in cortical areas 3b and 1 using identical random probe stimuli. STRFs of peripheral afferents consist of a rapidly appearing excitatory region followed by an in-field (replacing) inhibitory region. STRFs of SA1 afferents also exhibit flanking (surround) inhibition that can be attributed to skin mechanics. Cortical STRFs had longer time courses and greater inhibition compared with peripheral afferent STRFs, with less replacing inhibition in area 1 neurons compared with area 3b neurons. The greater inhibition observed in cortical STRFs point to the existence of underlying intracortical mechanisms. In addition, the shapes of excitatory and inhibitory lobes of both peripheral and cortical STRFs remained mostly stable over time, suggesting that their feature selectivity remains constant throughout the time course of the neural response. Finally, the gradual increase in the proportion of surround inhibition from the periphery to area 3b to area 1, and the concomitant decrease in response linearity of these neurons indicate the emergence of increasingly feature-specific response properties along the somatosensory pathway.

Figure 1.

A typical STRF. A, A single slice of the STRF from area 3b unit at t = 15 ms. Each pixel represents one probe in the 20 × 20 stimulator array, covering a 1 cm² area on the fingerpad (see Materials and Methods). The value at each probe location in the STRF slice indicates the change in firing rate per micrometer unit indentation (in spikes per second per micrometer) at time t₀ when a probe is indented at that location at time t = t₀ − 15 ms. Excitatory pixels are shown in red, and inhibitory pixels are shown in blue. The STRF is viewed as if looking down on the distal fingerpad, with the long axis of the finger pointing upward. B, The middle panel depicts the evoked response to the STRI stimulus (magenta) and the linear prediction (black) of the STRF of the same area 3b neuron during a 3 s time window. The panels above and below illustrate the computation of the predicted response at two time instants indicated by the arrows. In each frame, the STRI stimulus (grayscale) is superimposed over the STRF (color; excitatory pixels in red; inhibitory pixels in blue). Darker grayscale pixels indicate larger indentations. The predicted response at time t is computed by taking the pixel-by-pixel product of the STRF at each instant with the corresponding stimulus frame, and summing the result over a 50 ms time window before time t. Top panel, An increase in firing rate is predicted by the STRF when the probes stimulate the excitatory region of the receptive field. Bottom panel, A decrease in firing rate is predicted when the probes stimulate the inhibitory region. C, Top panel, Measured indentation amplitude versus time for a probe in the center of the excitatory region (11th row from top and 14th column from left) during a 3 s time window (identical to B). Bottom panel, Normalized power spectrum for this probe computed over the duration of the entire stimulus.

Figure 2.

Typical peripheral and cortical STRFs. STRFs of a peripheral SA1 afferent (A) and a peripheral RA afferent (B). STRFs in primary somatosensory cortex (areas 3b and 1) could be broadly categorized into three types. C, An area 3b unit with a purely excitatory STRF. D, An area 3b unit with replacing inhibition. E, An area 1 unit with surround and replacing inhibition. Color bars indicate pixel intensities in spikes per second per micrometer.

Figure 3.

Peripheral and cortical STRF areas. A, Cumulative histogram of the total area occupied by the STRF on the distal fingerpad (total probe area, 100 mm²). Total area is calculated as the area occupied by all STRF pixels significantly different from zero. B, Relationship between inhibitory and excitatory areas. Blue dots, peripheral SA1; red dots, peripheral RA; magenta crosses, cortical area 3b; green crosses, cortical area 1. Ellipses of the corresponding color indicate the area enclosed by 95% of the data, assuming a Gaussian distribution with the observed mean and covariance.

Figure 4.

Temporal evolution of STRF areas. A, Total (excitatory plus inhibitory) STRF area as a function of time, averaged over all neurons of a given afferent type or cortical area. B, Average areas of excitatory (solid lines) and inhibitory (dotted lines) regions over time for peripheral SA1 and RA afferents. C, Average areas of excitatory (solid lines) and inhibitory (dotted lines) regions over time for cortical areas 3b (magenta) and 1 (green).

Figure 5.

Peripheral and cortical STRF volumes. A, Inhibitory versus excitatory volumes (i.e., mass summed over all delays), in logarithmic scale. For a description of the symbols, see Figure 3. B, Average excitatory (solid lines) and inhibitory (dotted lines) mass as a function of time for peripheral afferents (top panel) and in areas 3b and 1 (bottom panel).

Figure 6.

Ratio of inhibitory to excitatory volume. I/E ratio is computed as the ratio between total inhibitory volume to the total excitatory volume. For a description of the symbols, see Figure 3.

Figure 7.

Properties of replacing inhibition. A, Cumulative histogram of the proportion of inhibitory volume that constituted replacing inhibition in each STRF. B, Cumulative histogram of the temporal duration of replacing inhibition. For a description of the symbols, see Figure 3.

Figure 8.

Temporal evolution of excitatory and inhibitory lobe aspect ratios. Average aspect ratios were computed at each time slice for excitatory (solid lines) and inhibitory regions (dotted lines), for peripheral afferents (top panel) and for cortical areas 3b and 1 (bottom panel). For a description of the symbols, see Figure 3.

Figure 9.

Peripheral and cortical STRF performance. STRF performance is measured as the correlation coefficient between the STRF model prediction and the observed response. For a description of the symbols, see Figure 3.

Figure 10.

Comparison of STRF area with punctate probe receptive field areas. Punctate probe RF area plotted against STRF total area. Data are shown for SA1 afferents (blue dots), RA afferents (red dots), area 3b neurons (magenta crosses), and area 1 neurons (green crosses). Ellipses of the corresponding color indicate the area enclosed by 95% of the data, assuming a Gaussian distribution with the observed mean and covariance.

Figure 11.

Response mean and variability. Firing rate variance versus mean firing rate plotted for peripheral and cortical responses to the STRI stimulus. Firing rate mean and variance were computed over three repeats for each 10 ms bin, and then averaged over the entire 200 s of the response. Data are from protocol B (see Materials and Methods). The solid black line indicates the unity line. Blue dots, SA1 afferents; red dots, RA afferents; magenta crosses, area 3b neurons; green crosses, area 1 neurons.

Figure 12.

Effect of indentation density on peripheral and cortical firing rates. Population average firing rates of SA1 (blue; dots) and RA (red; dots) afferents, and those of area 3b (magenta; crosses) and area 1 (green; crosses), are shown as a function of the stimulus indentation density (shown in logarithmic scale). Data are from protocol B.