Clutter substantially reduces selectivity for peripheral faces in the macaque brain.

According to a prominent view in neuroscience, visual stimuli are coded by discrete cortical networks that respond preferentially to specific categories, such as faces or objects. However, it remains unclear how these category-selective networks respond when viewing conditions are cluttered, i.e., when there is more than one stimulus in the visual field. Here, we asked three questions: (1) Does clutter reduce the response and selectivity for faces as a function of retinal location? (2) Is the preferential response to faces uniform across the visual field? And (3) Does the ventral visual pathway encode information about the location of cluttered faces? We used fMRI to measure the response of the face-selective network in awake, fixating macaques (2 female, 5 male). Across a series of four experiments, we manipulated the presence and absence of clutter, as well as the location of the faces relative to the fovea. We found that clutter reduces the response to peripheral faces. When presented in isolation, without clutter, the selectivity for faces is fairly uniform across the visual field, but, when clutter is present, there is a marked decrease in the selectivity for peripheral faces. We also found no evidence of a contralateral visual field bias when faces were presented in clutter. Nonetheless, multivariate analyses revealed that the location of cluttered faces could be decoded from the multivoxel response of the face-selective network. Collectively, these findings demonstrate that clutter blunts the selectivity of the face-selective network to peripheral faces, although information about their retinal location is retained.SIGNIFICANCE STATEMENTNumerous studies that have measured brain activity in macaques have found visual regions that respond preferentially to faces. Although these regions are thought to be essential for social behavior, their responses have typically been measured while faces were presented in isolation, a situation atypical of the real world. How do these regions respond when faces are presented with other stimuli? We report that, when clutter is present, the preferential response to foveated faces is spared but preferential response to peripheral faces is reduced. Our results indicate that the presence of clutter changes the response of the face-selective network.

The cortical and subcortical correlates of face pareidolia in the macaque brain.

Face detection is a foundational social skill for primates. This vital function is thought to be supported by specialized neural mechanisms; however, although several face-selective regions have been identified in both humans and nonhuman primates, there is no consensus about which region(s) are involved in face detection. Here, we used naturally occurring errors of face detection (i.e. objects with illusory facial features referred to as examples of 'face pareidolia') to identify regions of the macaque brain implicated in face detection. Using whole-brain functional magnetic resonance imaging to test awake rhesus macaques, we discovered that a subset of face-selective patches in the inferior temporal cortex, on the lower lateral edge of the superior temporal sulcus, and the amygdala respond more to objects with illusory facial features than matched non-face objects. Multivariate analyses of the data revealed differences in the representation of illusory faces across the functionally defined regions of interest. These differences suggest that the cortical and subcortical face-selective regions contribute uniquely to the detection of facial features. We conclude that face detection is supported by a multiplexed system in the primate brain.

Parallel Processing of Facial Expression and Head Orientation in the Macaque Brain.

When we move the features of our face, or turn our head, we communicate changes in our internal state to the people around us. How this information is encoded and used by an observer's brain is poorly understood. We investigated this issue using a functional MRI adaptation paradigm in awake male macaques. Among face-selective patches of the superior temporal sulcus (STS), we found a double dissociation of areas processing facial expression and those processing head orientation. The face-selective patches in the STS fundus were most sensitive to facial expression, as was the amygdala, whereas those on the lower, lateral edge of the sulcus were most sensitive to head orientation. The results of this study reveal a new dimension of functional organization, with face-selective patches segregating within the STS. The findings thus force a rethinking of the role of the face-processing system in representing subject-directed actions and supporting social cognition.SIGNIFICANCE STATEMENT When we are interacting with another person, we make inferences about their emotional state based on visual signals. For example, when a person's facial expression changes, we are given information about their feelings. While primates are thought to have specialized cortical mechanisms for analyzing the identity of faces, less is known about how these mechanisms unpack transient signals, like expression, that can change from one moment to the next. Here, using an fMRI adaptation paradigm, we demonstrate that while the identity of a face is held constant, there are separate mechanisms in the macaque brain for processing transient changes in the face's expression and orientation. These findings shed new light on the function of the face-processing system during social exchanges.