Amygdala controls saccade and gaze physically, motivationally, and socially

Abstract

Highlights-Central amygdala facilitates contralateral saccades selectively. -Saccade facilitation is related to motivational goals and social interaction. -The amygdala thus controls goal-directed behavior based on emotional contexts. AbstractThe amygdala is uniquely sensitive to emotional events. However, it is not understood whether and how the amygdala uses such emotional signals to control behavior, especially eye movements. We therefore injected muscimol (GABA A agonist) into the central nucleus of amygdala (CeA) in monkeys. This unilateral temporary inactivation suppressed saccades to contralateral but not ipsilateral targets, resulting in longer latencies, hypometric amplitudes, and slower velocity. During free viewing of movies, gaze was distributed mostly in the ipsilateral hemifield. Moreover, CeA inactivation disrupted the tendency of gaze toward social interaction images, which were normally focused on continuously. Conversely, optogenetic stimulation of CeA facilitated saccades to the contralateral side. These findings suggest that CeA controls spatially selective gaze and attention in emotional contexts, and provide a new framework for understanding psychiatric disorders related to amygdala dysfunction.

Primate Amygdalo-Nigral Pathway for Boosting Oculomotor Action in Motivating Situations

“…Together with our previous findings (Maeda et al, 2018(Maeda et al, , 2019, these results suggest that the amygdala governs social and emotional behaviors at multiple levels. At the most general level, the amygdala mediates contextappropriate social orienting, as evidenced by the effect of amygdala inactivation during movie free viewing (Maeda et al, 2019). At a more fine-grained level, the amygdala selectively mediates the spatially oriented action required for finding objects of interest quickly and accurately.…”

“…Our data showed that inactivation of the amygdala suppressed oculomotor behaviors. However, this effect might be caused by the inactivation of surrounding areas, especially the caudal-ventral part of the putamen, which we call ''putamen tail (PUTt)'' where neurons encode stable object values (Kunimatsu et al, 2019). We thus injected muscimol in PUTt unilaterally (monkey S: n = 3, monkey D: n = 4) (Figure S2A).…”

“…Consistent with this result, our pharmacological inactivation data showed that the amygdala inactivation suppressed saccades physically and motivationally (see Figures 1 and 2). Previous studies have revealed that neurons in the striatum (caudate nucleus and putamen) respond to many visual objects phasically and also encode the historical values of objects (Kim and Hikosaka, 2013;Kunimatsu et al, 2019;Yamamoto et al, 2013). The striatal neurons that have GABAergic (g-aminobutyric-acid-releasing) projections to SNr control oculomotor behaviors based on the object information (Hikosaka et al, 2000;.…”

“…The striatum includes the following characteristic activities. Medium spiny neurons were identified by their low baseline activity (1-10 Hz) and broad action potentials (Kunimatsu et al, 2019). Tonically active neurons exhibited a characteristic tonic firing pattern and wider action potentials.…”