Coding of vocalizations by single neurons in ventrolateral prefrontal cortex

Abstract

Neuronal activity in single prefrontal neurons has been correlated with behavioral responses, rules, task variables and stimulus features. In the non-human primate, neurons recorded in ventrolateral prefrontal cortex (VLPFC) have been found to respond to species-specific vocalizations. Previous studies have found multisensory neurons which respond to simultaneously presented faces and vocalizations in this region. Behavioral data suggests that face and vocal information are inextricably linked in animals and humans and therefore may also be tightly linked in the coding of communication calls in prefrontal neurons. In this study we therefore examined the role of VLPFC in encoding vocalization call type information. Specifically, we examined previously recorded single unit responses from the VLPFC in awake, behaving rhesus macaques in response to 3 types of species-specific vocalizations made by 3 individual callers. Analysis of responses by vocalization call type and caller identity showed that ∼19% of cells had a main effect of call type with fewer cells encoding caller. Classification performance of VLPFC neurons was ∼42% averaged across the population. When assessed at discrete time bins, classification performance reached 70 percent for coos in the first 300 ms and remained above chance for the duration of the response period, though performance was lower for other call types. In light of the sub-optimal classification performance of the majority of VLPFC neurons when only vocal information is present, and the recent evidence that most VLPFC neurons are multisensory, the potential enhancement of classification with the addition of accompanying face information is discussed and additional studies recommended. Behavioral and neuronal evidence has shown a considerable benefit in recognition and memory performance when faces and voices are presented simultaneously. In the natural environment both facial and vocalization information is present simultaneously and neural systems no doubt evolved to integrate multisensory stimuli during recognition. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".

Figure 1

The spectrograms and waveforms for the 9 vocalizations used in the current study are shown. There are three exemplars for each vocalization type (Coos, Grunts and Girneys) that were given by 3 callers in rows A, B and C. The calls have been previously characterized according to acoustic features, functional referents and the identity of the callers (Hauser and Marler, 1993; see Methods).

Figure 2

Individual VLPFC neurons demonstrated a range of selectivity to the 9 vocalizations. A) An auditory responsive neuron selective for two vocalizations but not call type or caller specific (coo 1 and grunt 3); B) A neuron that had the best response to all of the grunt exemplars; C) A neuron which was responsive to > 5 vocalizations but had the highest mean response to coo1 and grunt 1 from the same caller. D) An example of a neuron with a low selectivity score which was responsive to all 9 vocalizations but with the highest average response to two of the grunt exemplars. Error bars are standard error of the mean.

Figure 3

The neural response of three cells to the 9 vocalizations is shown as rasters and spike density functions. For each plot, the pre-stimulus fixation period (-250 to 0) occurs prior to the onset of the vocalization which occurs at time 0 and the response is shown over 800 ms. A) An example of a call type neuron with responses to the 3 coos (black) and 3 grunts (red). The response to the coos is bi-phasic and similar across coos but different from the grunts. In B and C the response to the 9 vocalizations is grouped by the three vocalization types (coos-black, grunts-red, girneys-blue). B) An example of a call type neuron with the highest average firing rate to grunts and the lowest response to coos. C) A call type responsive neuron which responded best to grunts.

Figure 4

Neuronal Consensus Trees. Consensus tree, based on the dendrograms for the individual call type responsive cells is shown. Dendrograms were derived for each of the 15 call type cells and their response to the 9 vocalizations (3 calls each from 3 callers) and a consensus tree was generated indicating the common groupings. The consensus tree indicated that in this sample 3 main groupings occurred: Grunt1 and Grunt 2 clustered together in 3 cells; Grunt 2 and Girney3 clustered together in 4 cells and Coo2 and Coo3 evoked a similar response in 3 cells.

Figure 5

Classification performance as a function of time bin length. This line graph shows how well VLPFC vocalization responsive neurons (n=37) categorized vocalizations as coo, grunt and girney using time bins of 60, 100, 150, 300 ms or a single 600 ms time bin. Utilization of small to medium bin sizes leads to decoding above chance levels, whereas using one larger bin size of 600 ms is less accurate. Error bars are standard error of the means.

Figure 6

Classification performance of call types over the course of the stimulus response period. Decoding performance at 4 × 150 ms time bins of VLPFC vocalization responsive neurons (n=37) is shown for each of the three call types. On average, cells are more accurate in their classification of coos and this is apparent in the first 300 ms of the response period. While the performance for grunts was above chance at 450 ms, girneys were not discriminated above chance (33.3%).