Gongchen Yu¹, Leor Katz¹, Richard Krauzlis¹; ¹Laboratory of Sensorimotor Research, National Eye Institute, NIH

The fast processing of faces and emotionally salient facial expressions is important for primate behavior and has long been proposed to rely on a subcortical visual pathway connecting the superior colliculus (SC), pulvinar, and amygdala. Despite the prominence of this hypothesis, there is no direct neuronal evidence (to our knowledge) for facial-expression processing in the SC. We recently reported that SC neurons show a robust preference for face images at extremely short latencies, raising the possibility that expression-specific information may also be present at these early processing stages. To test this idea, we recorded neuronal activity from the macaque SC while presenting images with a range of facial expressions, including images shown to evoke expression-selective activity in the amygdala. We found that a subset of SC neurons (10–15%) exhibited a short-latency (~50ms) modulation by facial expressions. Most of the expression-selective neurons responded most strongly to images that contained expressions of either threat or fear. By comparison, the short-latency face preference (replicated here) was found in ~50% of our visually responsive neurons. Our findings show that the primate SC not only encodes the presence of a face, but also key aspects of its emotional expression, and that this encoding takes place at remarkably short latencies. By demonstrating early expression-selective signals within the SC, our results fill a critical missing link in the proposed subcortical pathway for rapid evaluation of emotionally salient faces and inform models of how subcortical circuits support fast social perception.

Acknowledgements: This work is supported by the National Eye Institute Intramural Research Program at the National Institutes of Health ZIA EY000511.