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. 2014 Feb;9(2):209-17.
doi: 10.1093/scan/nss123. Epub 2012 Nov 21.

Reversible Inactivation of pSTS Suppresses Social Gaze Following in the Macaque (Macaca Mulatta)

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Free PMC article

Reversible Inactivation of pSTS Suppresses Social Gaze Following in the Macaque (Macaca Mulatta)

Arani Roy et al. Soc Cogn Affect Neurosci. .
Free PMC article

Abstract

Humans and other primates shift their attention to follow the gaze of others [gaze following (GF)]. This behavior is a foundational component of joint attention, which is severely disrupted in neurodevelopmental disorders such as autism and schizophrenia. Both cortical and subcortical pathways have been implicated in GF, but their contributions remain largely untested. While the proposed subcortical pathway hinges crucially on the amygdala, the cortical pathway is thought to require perceptual processing by a region in the posterior superior temporal sulcus (pSTS). To determine whether pSTS is necessary for typical GF behavior, we engaged rhesus macaques in a reward discrimination task confounded by leftward- and rightward-facing social distractors following saline or muscimol injections into left pSTS. We found that reversible inactivation of left pSTS with muscimol strongly suppressed GF, as assessed by reduced influence of observed gaze on target choices and saccadic reaction times. These findings demonstrate that activity in pSTS is required for normal GF by primates.

Keywords: autism; face-selective neurons; gaze following; joint attention; superior temporal sulcus.

Figures

Fig. 1
Fig. 1
(a) Schematic of the reward discrimination task and block structure. For details about the task see ‘Materials and Methods’ section. (b) Choice curves for left target choice from a single session; reward for left target increases along x-axis; top: monkey M1, bottom: monkey M2. In both monkeys choice for left target reliably increased with increasing reward size, but the choice curves for cue-left (red) and cue-right (blue) trials were shifted from each other along the x-axis. (c) Mean ± SEM PSEs for cue-left and cue-right trials, pooled data from two monkeys. (d) Single-session and mean ± SEM ΔPSE values from two monkeys. (e) Normalized saccade RT showing interaction of reward congruency and cue congruency. Cue-congruent saccades were faster than cue-incongruent ones, but only when made toward the low-reward targets.
Fig. 2
Fig. 2
(a) The 10°-angled grid in sideview (top) and topview (bottom) showing the layout of channels. The grid was positioned such that the angled channels pointed in the lateral direction (arrow, top). Center of the grid (marked X, bottom) was located 3-mm posterior and 12-mm lateral to IA0. Two channels in M1 (red) and three channels in M2 (green) were used for electrophysiology and muscimol injections. Anterior (A), posterior (P), medial (M) and lateral (L) directions are shown. (b) Firing rates of two pSTS neurons selective for left (top) and right (bottom) face orientations. (c) Firing rates of two pSTS neurons selective for straight face (top) and objects (bottom).
Fig. 3
Fig. 3
Two successive coronal sections (0.5-mm thickness) from structural MRI scans in monkey M1 and M2 showing approach of electrode tracks toward left pSTS. In the top section, a schematic (not drawn to scale) of the angular grid shows the electrode path extending to pSTS. Matching reference images from an online macaque brain atlas (source: http://brainmaps.org/index.php?action=viewslides&datid=141&start=1) shown below the MRI scans identify the scans in M1 and M2 to lie at −2 and 2 mm from interaural plane, respectively. LIP: lateral intraparietal sulcus; LS: lateral sulcus.
Fig. 4
Fig. 4
(a) Mean ± SEM PSEs for cue-left and cue-right trials following saline and muscimol injections in pSTS, pooled data from two monkeys. (b) Single-session and mean ± SEM ΔPSE values from saline and muscimol sessions, pooled from two monkeys. (c) Normalized saccade RTs showing reward × cue congruency interactions for saline and muscimol sessions. (d) Normalized saccade RTs for trials with neutral cue (gray square), under saline and muscimol conditions. Note the bigger error bars compared to facial cue trials in (c), due to the sample size for neutral cues being ∼1/10 that of facial cues.

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