The role of the right superior temporal gyrus in stimulus-centered spatial processing

Abstract

Although emerging neuropsychological evidence supports the involvement of temporal areas, and in particular the right superior temporal gyrus (STG), in allocentric neglect deficits, the role of STG in healthy spatial processing remains elusive. While several functional brain imaging studies have demonstrated involvement of the STG in tasks involving explicit stimulus-centered judgments, prior rTMS studies targeting the right STG did not find the expected neglect-like rightward bias in size judgments using the conventional landmark task. The objective of the current study was to investigate whether disruption of the right STG using inhibitory repetitive transcranial magnetic stimulation (rTMS) could impact stimulus-centered, allocentric spatial processing in healthy individuals. A lateralized version of the landmark task was developed to accentuate the dissociation between viewer-centered and stimulus-centered reference frames. We predicted that inhibiting activity in the right STG would decrease accuracy because of induced rightward bias centered on the line stimulus irrespective of its viewer-centered or egocentric locations. Eleven healthy, right-handed adults underwent the lateralized landmark task. After viewing each stimulus, participants had to judge whether the line was bisected, or whether the left (left-long trials) or the right segment (right-long trials) of the line was longer. Participants repeated the task before (pre-rTMS) and after (post-rTMS) receiving 20 min of 1 Hz rTMS over the right STG, the right supramarginal gyrus (SMG), and the vertex (a control site) during three separate visits. Linear mixed models for binomial data were generated with either accuracy or judgment errors as dependent variables, to compare 1) performance across trial types (bisection, non-bisection), and 2) pre- vs. post-rTMS performance between the vertex and the STG and the vertex and the SMG. Line eccentricity (z = 4.31, p < 0.0001) and line bisection (z = 5.49, p < 0.0001) were significant predictors of accuracy. In the models comparing the effects of rTMS, a significant two-way interaction with STG (z = -3.09, p = 0.002) revealed a decrease in accuracy of 9.5% and an increase in errors of the right-long type by 10.7% on bisection trials, in both left and right viewer-centered locations. No significant changes in leftward errors were found. These findings suggested an induced stimulus-centered rightward bias in our participants after STG stimulation. Notably, accuracy or errors were not influenced by SMG stimulation compared to vertex. In line with our predictions, the findings provide compelling evidence for right STG's involvement in healthy stimulus-centered spatial processing.

Gray Matter Alterations in Parkinson's Disease With Rapid Eye Movement Sleep Behavior Disorder: A Meta-Analysis of Voxel-Based Morphometry Studies

“…In summary, although brainstem abnormality is found to be associated with the promotion of idiopathic RBD from experimental and clinical perspectives (Scherfler et al, 2011;Hanyu et al, 2012), there are no apparent volume changes of GM in the brainstem in PD patients with RBD compared with those without RBD. Previous studies have demonstrated the strong association of reduced GM volume changes in the right STG with weakened spatial processing (Ellison et al, 2004;Gharabaghi et al, 2006;Shah-Basak et al, 2018), narcolepsy (Joo et al, 2009;Weng et al, 2015), impaired emotion processing to support social interactions (Muller et al, 2008;Pan et al, 2015;Van de Vliet et al, 2018;Zhang et al, 2018), violent behaviors (Zhang et al, 2019), and some psychiatric disorders (Moreira et al, 2017;Zhao et al, 2017;Wang et al, 2018). Consistent with our result, sleep disorders and nocturnal violence in PD patients with RBD can be partially explained by GM volume reduction in the right STG.…”

“…Previous studies have demonstrated the strong association of reduced GM volume changes in the right STG with weakened spatial processing (Ellison et al, 2004 ; Gharabaghi et al, 2006 ; Shah-Basak et al, 2018 ), narcolepsy (Joo et al, 2009 ; Weng et al, 2015 ), impaired emotion processing to support social interactions (Muller et al, 2008 ; Pan et al, 2015 ; Van de Vliet et al, 2018 ; Zhang et al, 2018 ), violent behaviors (Zhang et al, 2019 ), and some psychiatric disorders (Moreira et al, 2017 ; Zhao et al, 2017 ; Wang et al, 2018 ). Consistent with our result, sleep disorders and nocturnal violence in PD patients with RBD can be partially explained by GM volume reduction in the right STG.…”

Proactive engagement of cognitive control modulates implicit approach-avoidance bias

“…Thus, such decrease in activation is associated with more careful behavioral adjustment in response to the social stimulus, presumably to minimize error (i.e., executing the opposite action). Specifically, premotor areas (BA 6) and anterior cingulate cortex have been shown to activate parametrically to the neural computations of goal-directed actions (Fincham, Carter, Van Veen, Stenger, & Anderson, 2002;Gardini et al, 2016), while superior temporal regions have been robustly involved in visuo-spatial processing supporting motor planning (Hanakawa, Dimyan, & Hallett, 2008;Shah-Basak, Chen, Caulfield, Medina, & Hamilton, 2018). Overall, this is consistent with the down-regulation of a spatial processing and motor planning neural network likely to track the mental set of the prepotent stimulus-response behavior.…”

Callosal anisotropy predicts attentional network changes after parietal inhibitory stimulation

“…Support for STG involvement in spatial attention comes from neglect patients in whom impaired functional connectivity between STG and middle frontal gyrus (MFG) has been shown to correlate with the impaired interhemispheric parietal connectivity, which is in turn associated with the severity of the attentional deficit (He et al 2007). Consistent with lesion studies (Verdon et al, 2010) and both fMRI and TMS in healthy individuals (Galati et al, 2000;Neggers et al, 2006;Shah-Basak et al, 2018), STG inhibition by TMS affects allocentric, object-based, spatial processing (Ellison et al, 2004;Shah-Basak et al, 2018). It is noteworthy that the left STG cluster which increased RSFC with the right PPC seed is close to Heschl's gyrus, where early cortical auditory processing occurs (Tzourio et al, 1997).…”