Multi-finger receptive field properties in primary somatosensory cortex: A revised account of the spatiotemporal integration functions of area 3b

Abstract

The leading view in the somatosensory system indicates that area 3b serves as a cortical relay site that primarily encodes (cutaneous) tactile features limited to individual digits. Our recent work argues against this model by showing that area 3b cells can integrate both cutaneous and proprioceptive information from the hand. Here, we further test the validity of this model by studying multi-digit (MD) integration properties in area 3b. In contrast to the prevailing view, we show that most cells in area 3b have a receptive field (RF) that extends to multiple digits, with the size of the RF (i.e., the number of responsive digits) increasing across time. Further, we show that MD cells' orientation angle preference is highly correlated across digits. Taken together, these data show that area 3b plays a larger role in generating neural representations of tactile objects, as opposed to just being a "feature detector" relay site.

Keywords: CP: Neuroscience; RF; area 3b; cross-finger; haptics; integration; monkey; multi-digit; multi-finger; non-human primate; orientation; receptive field; somatosensory.

Figure 1.. Experimental setup

Animals set in a custom-made chair with their hand supinated and secured. Bars with different orientations were systematically delivered to digits 2–5 while animals were engaged in a visual contrast discrimination task. Animals were trained to fixate on a green triangle and saccade to the flanking circle with highest brightness. After animals were fully trained on the visual task, we recorded single-unit activity from the distal representation of area 3b.

Figure 2.. Majority of cells in area 3b have RFs spanning multiple digits

(A) Examples neurons from an RF spanning one (top row), two (second row), three (third row), or four (bottom row) digits. The insets in each graph show action potential waveforms recorded to each stimulated digit. (B) RF size distribution across the recorded population. Most cells had an RF covering two or more digits (~57% of cells). However, cells with an SD had the largest incidence (~43%), whereas cells with a four-digit RF had the lowest incidence (~10%). (C) Firing rates to stimulation on the preferred digit increased as a function of cells’ RF size. The graph shows violin plots of the normalized firing rate (R) distribution for each RF size condition. Each dot represents a cell’s mean R. *p < 0.01.

Figure 3.. Response variability in preferred digits increases with RF digit size

(A) Percentage of cells with a particular digit eliciting a higher response compared with remaining digits. Differences in response magnitude between the preferred and non-preferred digits increased as a function of RF size. We also found a slight decrease in percentage of cells with a unique preferred digit as a function of digit RF size (~73% of two-digit MD cells; ~69% of three-digit MD cells, and ~67% of four-digit MD cells). The inset represents the population response (average activity across recorded cells) to tactile stimulation to each digit for cells with two digits (left inset), three digits (center inset), and four digits (right inset). (B) Cumulative distribution of the Fano factor response (variance/mean) to stimulation on the preferred digit across cells with difference digit RF size. The data show a systematic shift in the cumulative distribution across RF size, with four-digit RF cells having the largest Fano factor value. The inset shows the median Fano factor value across RF digit size. These data show higher response variability to tactile stimulation on the preferred digit as a function of cells’ RF digit size. *p < 0.05; #p < 0.1. Error bars represent standard error of the mean.

Figure 4.. Neural responses have faster onset and are more precise in MD cells

(A) The top graph shows the instantaneous firing rate on the preferred digit of four neurons with excited responses (two in the left panel, two in the right panel) with an SD RF (red trace) and an MD RF (blue trace). Note that the firing rate axes for SD and MD are plotted on the left and right axes, respectively. The lower panel shows the cumulative distribution of onset time for the preferred digit on SD (red traces) and MD (blue traces) cells with excited (solid trace) and inhibited (dashed trace) initial responses. The earliest activations were largely from cells with a response below baseline (i.e., inhibited). (B) Cumulative distribution of the coefficient of variation (CV) of the inter-spike interval (ISI). The CV of the ISI was lower (i.e., more regular) for MD vs. SD cells. The left shows the median CV of the ISI decreasing as a function of RF size. The right inset shows the median CV of the ISI in MD (blue bar) and SD (red bar) cells with a significant response during the initial 20 ms relative to stimulus onset. Error bars represent standard error of the mean.

Figure 5.. The digit size RF of cells increases across time

The top graphs show examples of neural responses to tactile stimulation on each digit of a cell with an RF spanning four digits. The lower panel shows the cumulative distribution of onset time for each responsive digit across MD cells. The graph shows a systematic shift in response onset times across responsive digits. The inset in the cumulative distribution shows the median response onset time for each responsive digit of MD cells. Error bars represent standard error of the mean.

Figure 6.. Orientation tuning properties of SD and MD cells

(A) Example orientation tuning curves in cells with one digit (top-left graph), two digits (top-right graph), three digits (bottom-left graph), and four digits RF (bottom-right graph). The dashed black line in MD cells shows the average product of the tuning functions between preferred and non-preferred digits. (B) The percentage of orientation-tuned cells with a one-, two-, three-, or four-digit RF. The graph indicates that orientation tuning was more prevalent in the preferred digit of cells with an SD vs. MD RF. (C) Orientation index (OI) in the preferred digit of cells with a one-, two-, three-, or four-digit RF. The data revealed greater orientation selectivity in SD vs. MD cells. (D) The left panel shows a polar plot of the difference in the preferred angle between preferred and non-preferred digits of orientation-tuned MD cells. Each line represents the length of the difference vector between preferred and non-preferred digits. The right panel shows the percentage of cells with an angular difference between 0° and 90°. Most MD cells have a preferred angle difference between preferred and non-preferred digits of 22.5°. *p < 0.01; ^p = 0.05. Error bars represent standard error of the mean.