Anterior Temporal Lobectomy Impairs Neural Classification of Body Emotions in Right Superior Temporal Sulcus and Reduces Emotional Enhancement in Distributed Brain Areas without Affecting Behavioral Classification

Abstract

Humans with amygdalar lesions show proportional reductions of the emotional response to facial expressions in the fusiform face area as well as deficits in emotion recognition from facial expressions. While processing of bodily expressions shares many similarities with facial expressions, there is no substantial evidence that lesions of the amygdala result in similar behavioral and neural sequelae. We combined behavioral assessment with functional neuroimaging in a group of male and female humans with unilateral anterior temporal lobe (ATL) resections, including the amygdala (right: = 10; left: = 10) and 12 matched controls. The objective was to assess whether the amygdala is crucial for the recognition of body expressions and for modulatory effects on distant areas during perception of body expressions. The behavioral results revealed normal performance in both patient groups on emotion categorization of body expressions. The neuroimaging results showed that ATL patients displayed no enhanced activations in right fusiform body area and left extrastriate body area and that left ATL patients additionally displayed no enhanced activations in right posterior superior temporal sulcus and right extrastriate body area, respectively. Multivoxel pattern analysis revealed altered categorization capacity between emotional and neutral stimuli in right posterior superior temporal sulcus in right ATL patients. In addition, we also found emotional enhancement in frontal, parietal, occipital, and cingulate regions in controls. Together, our data show that the amygdala and ATLs are not necessary for recognition of dynamic body expressions, but suggest that amygdala lesions affect body emotion processing in distant brain areas. For humans, information from emotional expressions of others is crucial to support social interactions. The majority of emotion studies has focused on facial expressions; however, in daily life, we also use information from body postures and body movement. Visual processing of body expressions relies on a brain network, including body-specific visual areas and visuomotor areas. Even though the importance of the amygdala and its modulatory effects on distant brain regions have been documented, it remains unclear whether the amygdala plays a crucial role in emotional body processing. By combining behavioral and neuroimaging data in patients with amygdalar lesions, we provide further evidence for its modulatory effect on distant areas during the perception of body expressions.

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.…”

Network level characteristics in the emotion recognition network after unilateral temporal lobe surgery

“…This contrasted with clear widespread changes in brain activation (mainly in temporal, parietal and cingulate cortex) and neural decoding (in the right posterior superior temporal sulcus) in TLS. We concluded that intact bilateral amygdalae are not necessary for successful recognition of body expressions (Van de Vliet et al., 2018). In the present study, we used the same dataset to investigate whether this preserved recognition is associated with compensatory changes in global network properties of the emotion recognition network by means of generalized psychophysiological interaction (gPPI) and graph theory.…”

“…At the behavioural level, amygdalectomy is associated with facial emotion recognition deficits (Monti & Meletti, 2015), but this is not a consistent finding (Adolphs, Tranel, Damasio, & Damasio, 1995; Fowler et al., 2006; Milesi et al., 2014). Furthermore, recognition of bodily expressions appears to be preserved following TLS (Atkinson, Heberlein, & Adolphs, 2007; Van de Vliet et al., 2018). At the neural level, inconsistent findings have also been reported regarding distant effects on emotional responses in TLS (Edmiston et al., 2013; Van de Vliet et al., 2018).…”

“…Furthermore, recognition of bodily expressions appears to be preserved following TLS (Atkinson, Heberlein, & Adolphs, 2007; Van de Vliet et al., 2018). At the neural level, inconsistent findings have also been reported regarding distant effects on emotional responses in TLS (Edmiston et al., 2013; Van de Vliet et al., 2018).…”