The causal link between neural activity in inferotemporal cortex and free viewing eye movements

Abstract

Eye movements are primarily driven by vision. Saliency map models that aim to predict eye movements rely on low-level visual information. However, the high-level structure of visual objects, such as a face, also plays a significant role in determining eye movements. This structure can only be identified and processed by the high-level areas of the ventral visual pathway. We hypothesized that perturbation of neurons in the inferior temporal (IT) cortex that are specifically responsive to certain categories of stimuli (e.g. faces) would alter eye movements during free viewing. In this study, we systematically studied the effect of inactivation of IT neurons, particularly face-selective units, on eye movements during free viewing of images from different object categories (including faces). First, we used fMRI to localize face- and object-selective patches in the IT cortex of two macaque monkeys. We then targeted these patches with microinjection of muscimol, a strong GABA receptor agonist. In each session, one hemisphere was targeted. The results showed that inactivation of the middle face patches did not affect the animals' attraction to faces during free viewing, as they still focused on the faces in the natural scenes presented to them. However, the pattern of eye movements within faces changed dramatically. Specifically, the animals spent less time looking at the ipsilateral eye relative to the targeted hemisphere. Injection of muscimol outside the face patch did not produce the same effect. These findings demonstrate the causal role of neural activity in the face-selective subregions of IT cortex in eye movements and strongly suggest existence of high-level, object-based saliency maps in the visual system.