Inactivation of face-selective neurons alters eye movements when free viewing faces

Abstract

During free viewing, faces attract gaze and induce specific fixation patterns corresponding to the facial features. This suggests that neurons encoding the facial features are in the causal chain that steers the eyes. However, there is no physiological evidence to support a mechanistic link between face-encoding neurons in high-level visual areas and the oculomotor system. In this study, we targeted the middle face patches of the inferior temporal (IT) cortex in two macaque monkeys using an functional magnetic resonance imaging (fMRI) localizer. We then utilized muscimol microinjection to unilaterally suppress IT neural activity inside and outside the face patches and recorded eye movements while the animals free viewing natural scenes. Inactivation of the face-selective neurons altered the pattern of eye movements on faces: The monkeys found faces in the scene but neglected the eye contralateral to the inactivation hemisphere. These findings reveal the causal contribution of the high-level visual cortex in eye movements.

A behavioral advantage for the face pareidolia illusion in peripheral vision

“…It follows that the primate brain may accumulate evidence for “resemblance to a face” judgements based on how many face-like features are present, with a particular emphasis on the presence of illusory eyes 20 , 22 . Interestingly, this theory is consistent with eye tracking studies in macaques showing that the illusory eyes, in examples of face pareidolia, attract a disproportionate amount of attention 14 , 40 , 42 . However, in the current study, the illusory eyes were available to participants in both the close and peripheral conditions.…”

“…This further indicates that the viewing behavior of the participants were driven by different visual properties and features depending on the distance of the choice stimuli from the initial fixation spot. More research is needed to understand the visual features that guide eye movements when stimuli are not presented in foveal, or near-foveal, vision (see 40 ). Even so, regardless of what visual properties promote the face pareidolia illusion, and whether these change across the visual field, overall our results reveal that ambient examples of face pareidolia bias viewing behavior towards peripheral locations.…”

“…For example, it has been shown that blindsight patients will preferentially orient their eyes towards the spatial location of face stimuli even when they do not report perceiving faces 54 – 57 . This might help explain mixed findings in the comparative literature; while macaque monkeys preferentially orient their eyes towards examples of face pareidolia in eye tracking studies 7 , 14 , 40 , it was recently reported that members of the same species that are conditioned to select faces, do not categorize ambient examples of face pareidolia as “faces” 58 . This implies that, while the macaque brain might initially mistake objects with illusory faces as being face-like, later processes decide that examples of face pareidolia are objects, not faces.…”

“…In the comparative literature, biases towards face pareidolia in eye tracking studies have been used to identify the neural mechanisms underlying face detection and prioritization. For example, it has been shown that while typically developing rhesus macaques preferentially look at examples of face pareidolia 14 , and illusory facial features 40 , 42 , in free viewing tasks, this implicit, untrained, behavior is eliminated following the bilateral removal of the amygdala 7 . This is further supported by neuroimaging studies showing that examples of face pareidolia activate the amygdala in the primate brain 11 , 13 .…”

“…Therefore, an implication that directly follows from the current results is that the human amygdala, a face-responsive subcortical region 43 , might play a causal role in detecting faces in the visual environment and guiding eye movements towards their location. Although studies have started to look at the impact of amygdala disruption on eye movements towards faces in human participants 44 , more research is needed to determine whether amygdala activity is sufficient for biasing oculomotor behavior towards faces or, alternatively, whether this bias is the consequence of interactions between the amygdala and other brain regions and circuits 40 .…”