Mirroring of attention by neurons in macaque parietal cortex

Abstract

Macaques, like humans, rapidly orient their attention in the direction other individuals are looking. Both cortical and subcortical pathways have been proposed as neural mediators of social gaze following, but neither pathway has been characterized electrophysiologically in behaving animals. To address this gap, we recorded the activity of single neurons in the lateral intraparietal area (LIP) of rhesus macaques to determine whether and how this area might contribute to gaze following. A subset of LIP neurons mirrored observed attention by firing both when the subject looked in the preferred direction of the neuron, and when observed monkeys looked in the preferred direction of the neuron, despite the irrelevance of the monkey images to the task. Importantly, the timing of these modulations matched the time course of gaze-following behavior. A second population of neurons was suppressed by social gaze cues, possibly subserving task demands by maintaining fixation on the observed face. These observations suggest that LIP contributes to sharing of observed attention and link mirror representations in parietal cortex to a well studied imitative behavior.gaze following ͉ imitation ͉ joint attention ͉ mirror neurons ͉ shared attention P eople naturally and intuitively share attention with each other. In a laboratory setting, people respond more quickly to targets that are the object of another's attention, even when this social cuing is brief or consistently misleading (1-3). Monkeys' attention also follows the gaze of others (4), and the similar magnitude and time course of gaze following by rhesus macaques and humans (5) implicates shared neural mechanisms. The ability to follow gaze is believed to be an important foundation for theory of mind (6, 7); thus, the neural processes governing gaze following are relevant both to the evolution of social cognition (8-10) and to clinical disorders, such as autism, associated with social attention deficits (11)(12)(13)(14). Although gaze following involves automatic ''mirroring'' of other's mental states, to our knowledge, mirror neurons (15, 16) for visual orienting have not previously been identified.Current evidence suggests that identification of where other individuals are looking is accomplished by neurons along the superior temporal sulcus (STS) (17)(18)(19)(20) (22), as well as the parietal cortex (28). These observations invite the simple hypothesis that gazefollowing behavior is mediated by a relatively straightforward system, beginning with the STS and proceeding directly to the attention-and gaze-control networks. Although intuitively appealing, this model raises several important questions.First, gaze-following behavior fits poorly into existing models of attention (1, 2), which dichotomize the underlying mechanism as either reflexively driven by exogenous stimuli or endogenously guided by internal goals (29, 30). Although there is some evidence that specific neural circuits mediate these processes (31-33), the precise contributions of neurons within different b...

The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations

“…The properties of mirror neurons located in area LIP have been described by Shepherd and colleagues 97 . They found that a set of LIP neurons fired both when the monkey looked in the neuron-preferred direction and when it saw another monkey looking in the same direction.…”

Visual attention and action: How cueing, direct mapping, and social interactions drive orienting

“…This work has revealed that, despite evidence for neural regions specialized for gaze processing, there has so far been little support for 'eye movement cells' with mirror properties. Recently, some support has emerged for the presence of mirror neurons in areas that control saccadic activity and overt attention such as the lateral intraparietal area (LIP; Shepherd, Klein, Deaner, & Platt, 2009), and the supplementary motor area including the supplementary eye fields (Mukamel et al, 2010). However, no evidence yet exists for neurons with mirror properties in areas that are specifically linked with eye movements such as the frontal eye fields.…”

“…However, no evidence yet exists for neurons with mirror properties in areas that are specifically linked with eye movements such as the frontal eye fields. Additionally, only Shepherd et al (2009) recorded mirror properties of cells specifically for observed and performed eye-movement behaviours. In contrast, mirror neurons which activate during the performance and observation of actions have been found throughout the premotor cortex (PMC), which is primarily responsible for planning a range of manual actions (CalvoMerino et al, 2005;Ferrari, Gallese, Rizzolatti, & Fogassi, 2003;.…”

Adaptations for social cognition in the primate brain

“…Inactivation of neurons in the STS using a drug to block neuronal spiking impairs gaze-following in rhesus macaques, consistent with a role in identifying the locus of other animals' attention [102]. Shifting attention in response to the direction in which another individual is looking appears to be mediated by 'mirror' neurons in the lateral intraparietal area (LIP) that respond both when monkeys look in a particular direction and when they observe another monkey look in the same direction [103], another example of embodied cognition. Together, these findings suggest that a circuit connecting STS, amygdala and LIP subserves rapid, reflexive gaze-following in nonhuman primates.…”