Variability of neuronal responses in the posterior superior temporal sulcus predicts choice behavior during social interactions.

Abstract

Recent studies have shown that neural activity in a well-defined patch in the posterior superior temporal sulcus (the "gaze-following patch," GFP) of the primate brain is strongly modulated when the other's gaze attracts the observer's attention to locations/objects, the other is looking at. Changes of the mean discharge rate of neurons in the monkey GFP indicate that they are involved in two distinct computations: the allocation of spatial attention guided by the other's gaze vector and the suppression of gaze following if inappropriate in a given situation. Here, we asked if and how the discharge variability of neurons in the GFP is related to the task and if it carries information on behavioral performance. To this end, we calculated the Fano factor as a measure of across-trial discharge variability as a function of time. Our results show that all neurons exhibiting a task-related discharge-rate modulation also exhibit a stimulus onset-dependent drop in the Fano factor. Furthermore, the amplitude of the Fano factor reduction is modulated by task condition and the neuron's selectivity in this regard. We found that these effects are directly related to the monkeys' behavioral performance in that the Fano factor is predictive about upcoming correct or wrong decisions. Our results indicate that neuronal discharge variability as gauged by the Fano factor, hitherto primarily studied in the context of visual perception or motor control, is an informative measure also in studies of the neural underpinnings of complex social behavior.NEW & NOTEWORTHY Quenching of neural variability following stimulus onset is a widely accepted phenomenon. However, the relevance of quenching for the shaping of complex social behaviors remains to be explored. Here, we show that task selective neurons in the GFP exhibit a higher degree of variability quenching than their neighboring unselective neurons. Furthermore, we demonstrate that behavioral errors are not only associated with lower firing rates but also less variability quenching, suggesting that both facilitate optimal performance.