Population Coding of Facial Information in the Monkey Superior Colliculus and Pulvinar

Abstract

The superior colliculus (SC) and pulvinar are thought to function as a subcortical visual pathway that bypasses the striate cortex and detects fundamental facial information. We previously investigated neuronal responses in the SC and pulvinar of monkeys during a delayed nonmatching-to-sample task, in which the monkeys were required to discriminate among 35 facial photos of five models and other categories of visual stimuli, and reported that population coding by multiple SC and pulvinar neurons well discriminated facial photos from other categories of stimuli (Nguyen et al., 2013, 2014). However, it remains unknown whether population coding could represent multiple types of facial information including facial identity, gender, facial orientation, and gaze direction. In the present study, to investigate population coding of multiple types of facial information by the SC and pulvinar neurons, we reanalyzed the same neuronal responses in the SC and pulvinar; the responses of 112 neurons in the SC and 68 neurons in the pulvinar in serial 50-ms epochs after stimulus onset were reanalyzed with multidimensional scaling (MDS). The results indicated that population coding by neurons in both the SC and pulvinar classified some aspects of facial information, such as face orientation, gender, and identity, of the facial photos in the second epoch (50–100 ms after stimulus onset). The Euclidean distances between all the pairs of stimuli in the MDS spaces in the SC were significantly correlated with those in the pulvinar, which suggested that the SC and pulvinar function as a unit. However, in contrast with the known population coding of face neurons in the temporal cortex, the facial information coding in the SC and pulvinar was coarse and insufficient. In these subcortical areas, identity discrimination was face orientation-dependent and the left and right profiles were not discriminated. Furthermore, gaze direction information was not extracted in the SC and pulvinar. These results suggest that the SC and pulvinar, which comprise the subcortical visual pathway, send coarse and rapid information on faces to the cortical system in a bottom-up process.

Organizing principles of pulvino-cortical connectivity in humans

“…These data are consistent with anatomical connectivity studies in macaques that demonstrated projections from the medial ventral pulvinar to the lower lip of the STS (Grimaldi et al, 2016) and projections from ventral temporal cortex (around area TF) to lateral portions of the pulvinar (Benevento and Rezak, 1976) as well as an electrical stimulation study showing evoked activity within the ventral medial pulvinar from stimulation of face patches in the lower bank of the STS (Moeller et al, 2008). Previous studies have demonstrated responsiveness in the primate pulvinar to object features at the neuronal level (Nguyen et al, 2013;Nguyen et al, 2016). To our knowledge, this is the first demonstration of image category-selective visual responses within the human thalamus.…”

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

“…To analyze representation of the stimulus by population activity of the SC neurons, activity of the SC neurons with central RFs (n = 32) was analyzed by MDS (Le et al, 2013(Le et al, , 2014Nguyen et al, 2013Nguyen et al, , 2014Nguyen et al, , 2016Dinh et al, 2018). MDS constructs a stimulus space in which relationships among stimuli are shown (Young, 1987).…”

The premotor syndrome of cervical dystonia: Disordered processing of salient environmental stimuli

“…) . Fast emotional face processing with responses in the amygdala at 74 ms has been demonstrated in epilepsy patients being evaluated for temporal lobectomy; in nonhuman primates, pulvinar recordings show 50‐ms latency responses to face‐like stimuli, including cartoon faces . The traditional conception of the function of the amygdala as a “fear hub” (responsive to visual images of fear alone) has been challenged by recent fMRI studies, which have shown that the amygdala was comparably active in response to facial emotional expressions indicating anger, disgust, fear, happiness, and sadness …”