The monkey pulvinar neurons differentially respond to emotional expressions of human faces

Recent psychological studies suggest that the amygdala is not essential for early stages of emotional facial processing, and that the colliculo-pulvinar pathway might play this role. Nevertheless, the actual role of pulvinar nucleus on the recognition of emotional faces remains obscure. In the present study, we recorded single-unit activity of pulvinar neurons in 2 monkeys during recognition of emotional faces in a delayed non-match-to-sample (DNMS) task, using human face stimuli with differing emotional expressions (sad, angry, happy, surprised and neutral) and simple geometric pattern control figures. A total of 184 single neurons from lateral and medial pulvinar have been sampled. From this total, 41 (22.2%) were found to be “visually responsive”, that is, responded to one or more of the visual stimuli. Among the visually responsive neurons, 23 responded non-differentially to all stimuli (facial stimuli and control). Another 18 responded differentially to facial identity and/or emotional expression. Response latencies of the pulvinar neurons to these facial stimuli ranged very widely; firing onsets for 16 (39.0%, 16/41) neurons were shorter than 100 ms, while for 13 (31.7%, 13/41) it was greater than 300 ms. The results thus indicate that 43.9% of the visually responsive pulvinar neurons differentially responded to the emotional expressions of the human faces. Furthermore, wide distribution of the response latencies of the pulvinar neurons suggests that pulvinar neurons might mediate intracortical connections as well as the fast subcortical pathway to the amygdala. These results highlight a role of the pulvinar in the processing of emotional facial stimuli.

Research highlights▶ Monkey pulvinar neurons responded differentially to photos of facial expression. ▶ Pulvinar neurons displayed short latency responses consistent with collicular inputs. ▶ The colliculo-pulvinar system might be involved in early stages of emotional facial processing.