Monkeys head-gaze following is fast, precise and not fully suppressible

Abstract

Human eye-gaze is a powerful stimulus, drawing the observer's attention to places and objects of interest to someone else ('eye-gaze following'). The largely homogeneous eyes of monkeys, compromising the assessment of eyegaze by conspecifics from larger distances, explain the absence of comparable eye-gaze following in these animals. Yet, monkeys are able to use peer head orientation to shift attention ('head-gaze following'). How similar are monkeys' head-gaze and human eye-gaze following? To address this question, we trained rhesus monkeys to make saccades to targets, either identified by the head-gaze of demonstrator monkeys or, alternatively, identified by learned associations between the demonstrators' facial identities and the targets (gaze versus identity following). In a variant of this task that occurred at random, the instruction to follow head-gaze or identity was replaced in the course of a trial by the new rule to detect a change of luminance of one of the saccade targets. Although this change-of-rule rendered the demonstrator portraits irrelevant, they nevertheless influenced performance, reflecting a precise redistribution of spatial attention. The specific features depended on whether the initial rule was head-gaze or identity following: head-gaze caused an insuppressible shift of attention to the target gazed at by the demonstrator, whereas identity matching prompted much later shifts of attention, however, only if the initial rule had been identity following. Furthermore, shifts of attention prompted by head-gaze were spatially precise. Automaticity and swiftness, spatial precision and limited executive control characterizing monkeys' head-gaze following are key features of human eye-gaze following. This similarity supports the notion that both may rely on the same conserved neural circuitry.

Following Eye Gaze Activates a Patch in the Posterior Temporal Cortex That Is not Part of the Human “Face Patch” System

“…However, this does not mean that it would not be subject to cognitive control. Indeed, careful psychophysical experiments on monkey head gaze-following (Marciniak et al, 2015), probably homologous to human gaze-following, clearly show that with the exception of a small early reflex component, a substantial part of the gaze-following response can be suppressed. Hence, we can be confident that the BOLD contrast used to identify the GFP reflects differences in gaze-following–related processing and its cognitive control.…”

“…This behavior emerges very early during the development of the individual (Tomasello and Carpenter, 2005; Tomasello et al, 2007). According to Marciniak et al (2015), it is characterized by key features that make human eye gaze-following reflexlike, namely swiftness and incomplete cognitive control. As described earlier, monkey head gaze-following activates a patch of cortex (the monkey GFP) whose location bilaterally in the posterior STS is reminiscent of the location of the human GFP.…”

Decoding of the other’s focus of attention by a temporal cortex module

“…It is also unclear if neurons in the GFP may possibly contribute to the cognitive control of gaze following, integrating contextual information relevant for the modulation of the behavior. After all, although human and monkey gaze following has features of a quasi reflex-like behavior that kicks in at short latency, it can be suppressed to a considerable degree if not appropriate within a given context (13,14).…”

Reflexive gaze following in common marmoset monkeys

“…By the same token the lack of high resolution behavioral data has as yet precluded well-founded inferences about the relationship of marmoset gaze following to gaze following exhibited by humans and rhesus monkeys, the two species of old world primates for which detailed behavioral and neuronal data are available [5,6]. Gaze following of macaques and humans is reflex-like in the sense that it is fast and hard to suppress, two features that have contributed to the assumption of a domain specific faculty [7–12] based on a dedicated neural system [13]. Do marmosets follow the gaze of conspecifics in the same reflex-like manner?…”