Behavioral context affects social signal representations within single primate prefrontal cortex neurons

Abstract

We tested whether social signal processing in more traditional, head-restrained contexts is representative of the putative natural analog-social communication-by comparing responses to vocalizations within individual neurons in marmoset prefrontal cortex (PFC) across a series of behavioral contexts ranging from traditional to naturalistic. Although vocalization-responsive neurons were evident in all contexts, cross-context consistency was notably limited. A response to these social signals when subjects were head-restrained was not predictive of a comparable neural response to the identical vocalizations during natural communication. This pattern was evident both within individual neurons and at a population level, as PFC activity could be reliably decoded for the behavioral context in which vocalizations were heard. These results suggest that neural representations of social signals in primate PFC are not static but highly flexible and likely reflect how nuances of the dynamic behavioral contexts affect the perception of these signals and what they communicate.

Keywords: faces; marmoset; natural communication; prefrontal cortex; primate; social signals; vocalizations.

Figure 1.. Behavioral Contexts and Recording Locations

(A) Drawings of the three behavioral contexts. (B) Distribution of phee responsive neurons in marmoset PFC for all three contexts. Black polygonal shape represents the outline of the four electrode arrays across three marmosets. Each dot represents one electrode channel and its ratio (indicated by the color bar) of phee responsive neurons relative to all single neurons recorded at that location. (C) Anatomical map of the frontal cortex. Gray square represents the zoomed in portion of PFC depicted in B. Colored squares represent the position and orientation of the four electrode arrays. Dashed lines = right hemisphere implants, Solid lines = left hemisphere. Color bar indicates the proportion of pheeresponsive neurons, which are shown in the colored dots in the anatomical map (D) Two-pulsed marmoset phee call is shown above a normalized PSTH with 95% Confidence Interval for all phee-responsive neurons. Gray boxes indicate the average duration of phee pulses.

Figure 2.. Within-Neuron Context Comparisons

(A) Venn Diagram shows the percentage of significant phee responsive neurons (n=170) for all combinations of behavioral contexts. (B) Exemplar PFC neurons showing within-neuron contextual selectivity observed in this population. Raster plots show neural responses to individual phee call trial presentations on each row, while the normalized PSTH is shown as a thick dark line for each context. Grey shading on each trial indicates the onset/offset of each phee call pulse or noise stimuli. (C) Exemplar PFC neuron exhibits contextual and stimulus selectivity (D) Scatter plots show the percent change in neural activity to phee calls relative to baseline in each paired combination of contexts for the 170 phee responsive neurons. Median firing rates are based on 30 phee call presentations in R and F and mean 46 (range 15–93) in C.

Figure 3.. Context Differences Across the Population

(A) Normalized firing rate to phee calls in each context (See STAR Methods). Single blue circles represent each individual phee-responsive neuron. The red line was constructed from the slope and intercept of the linear mixed effect model (B) Performance of neural decoder for RFC units and All Units in this population. (C) Distribution of MCC values for 100 randomly selected 26 non-RFC units from the population. The vertical red line plots the median MCC for RFC units. (D) Mean confusion matrix across 500 simulations decoders tested with only RFC units (left) and All Units (right). (E) t-SNE plot (t-Distributed Stochastic Neighbor Embedding) created by inputting the median performing simulation’s PCA. (F) Individual unit performance in decoding neural response in each behavioral context. 99.9% confidence intervals are shown but too small to be visible. Filled in points represent units with significantly higher response above chance in accuracy (p = 0.001). (G) Distribution of units that had significantly higher accuracy above chance (black) compared to below chance (white) binned across the category types from panel A. NS = not significant. * statistically significant.

Figure 4.. Social State Modulation of PFC

(A) Box plots show the normalized firing rate of neurons phee responsive neurons in the ‘Antiphonal’ and ‘Independent’ contexts. Single blue circles represent individual neurons. (B-Left) Performance of ‘Stimulus-Only’ and ‘State-Based’ neural decoders. (B-Right) Performance of PreStim and PostStim neural decoder. (C) Mean confusion matrix for decoder performance for Stimulus-Only (left) and State-Based (right). (D) Individual unit performance of units in the State-Based decoder. 109 neurons with accuracies above chance with 99.9% confidence are shown in black. 99.9% confidence interval bounds are plotted but are too small to be visible. * statistically significant.