Sensorimotor inhibition during emotional processing

Abstract

Visual processing of emotional stimuli has been shown to engage complex cortical and subcortical networks, but it is still unclear how it affects sensorimotor integration processes. To fill this gap, here, we used a TMS protocol named short-latency afferent inhibition (SAI), capturing sensorimotor interactions, while healthy participants were observing emotional body language (EBL) and International Affective Picture System (IAPS) stimuli. Participants were presented with emotional (fear- and happiness-related) or non-emotional (neutral) EBL and IAPS stimuli while SAI was tested at 120 ms and 300 ms after pictures presentation. At the earlier time point (120 ms), we found that fear-related EBL and IAPS stimuli selectively enhanced SAI as indexed by the greater inhibitory effect of somatosensory afferents on motor excitability. Larger early SAI enhancement was associated with lower scores at the Behavioural Inhibition Scale (BIS). At the later time point (300 ms), we found a generalized SAI decrease for all kind of stimuli (fear, happiness or neutral). Because the SAI index reflects integrative activity of cholinergic sensorimotor circuits, our findings suggest greater sensitivity of such circuits during early (120 ms) processing of threat-related information. Moreover, the correlation with BIS score may suggest increased attention and sensory vigilance in participants with greater anxiety-related dispositions. In conclusion, the results of this study show that sensorimotor inhibition is rapidly enhanced while processing threatening stimuli and that SAI protocol might be a valuable option in evaluating emotional-motor interactions in physiological and pathological conditions.

Early modulations of neural oscillations during the processing of emotional body language

“…Transcranial magnetic stimulation (TMS) studies have shown that static pictures of fearful EBL exert an inhibitory, rapid effect on corticospinal excitability as well as on intracortical facilitatory mechanisms within the primary motor cortex (M1) of the observer (Borgomaneri et al, 2015b, 2015c, 2017) when compared with positive EBL and nonemotional body movements. Furthermore, in a previous TMS work by our group, we found that fearful EBL stimuli, differently from positive and nonemotional stimuli, enhance short‐latency somatosensory afferent inhibition (SAI) at 120 ms after the stimulus onset, hence demonstrating that the observation of fearful EBL produces an early reduction of M1 excitability mediated by sensorimotor integration mechanisms involving the primary somatosensory cortex (S1) (Botta et al, 2022). Moreover, in behavioral tasks, EBL static pictures induced shorter response times, when compared with positive EBL and nonemotional body language (Borgomaneri et al, 2020; Botta et al, 2021).…”

“…This study aimed to test whether observation of EBL was able to modulate cortical activity in sensorimotor areas, specifically ERPs and cortical oscillations in the mu‐alpha and lower beta frequency bands, at short latencies (around 100 ms after the onset of the EBL stimulus). We built on our previous TMS findings that sensorimotor integration, as tested in M1 using the SAI protocol, is modulated during the processing of static images depicting fear EBL, already at 120 ms from the stimulus onset (Botta et al, 2022). Based on current knowledge of the neurophysiological cortico‐cortical mechanism underlying the SAI effect (Turco et al, 2018), and the increasing recognition of a key role of primary sensorimotor areas in the perception of others' actions and emotions (Adolphs et al, 2000; Bufalari et al, 2007; Gazzola et al, 2012; Keysers et al, 2010; Paracampo et al, 2017; Pitcher et al, 2008), we hypothesized that modulation of sensorimotor integration during observation of fear EBL was driven by increased activity in S1 – reflecting increased sensory vigilance – and an inhibitory effect on M1 excitability – reflecting a freezing response to potentially threatening signals.…”

“…Brain activity related to source space was reconstructed via the exact low‐resolution brain electromagnetic tomography (eLORETA) method (Cao et al, 2018; Pascual‐Marqui et al, 2011; Zhao et al, 2019). Considering previous studies (Botta et al, 2022; Sim et al, 2015) and the main research question we aimed to explore, the ROIs taken for the time‐frequency analysis were the left and right M1 (lM1 and rM1, respectively) and the left and right S1 (lS1 and rS1). Coordinates for each ROI were taken from the Neurosynth website (https://neurosynth.org/) based on the paper of Mayka and colleagues for the motor area (Mayka et al, 2006) and from Roux et al (2018) for the somatosensory area.…”

“…Summing up, considering the fast temporal dynamics of EBL processing (van Heijnsbergen et al, 2007), and in particular the early motor (Borgomaneri et al, 2015b, 2015c, 2017) and sensorimotor responses to fearful expressions (Botta et al, 2022), it seems plausible to expect a decreased M1 activity in response to fearful EBL in the temporal window of the P100 (Kiefer et al, 2011; Sim et al, 2015). We also expect to observe increased activity in the mu‐alpha and/or beta frequency bands over primary somatosensory areas in the early phases of fearful EBL processing at the expense of reduced activity over motor areas.…”

How emotional expressions motivate action

“…-License CC BYHashemi et al, 2019) and the basal ganglia (BG), and cortical, such as the primary(Borgomaneri et al, 2015(Borgomaneri et al, , 2021Botta et al, 2022;Ferrari et al, 2021;Hortensius et al, 2016;Schutter et al, 2008) and secondary motor cortices (i.e., the supplementary motor (SMA) and premotor (PM) cortex;Diano et al, 2017;Grèzes et al, 2014; Grèzes & Dezecache, 2014;Rizzo et al, 2018;Rolls et al, 2022), as well as to the cerebellum(Pierce & Péron, 2020), influencing action readiness.Other than via the AMY and other subcortical centers, the PUL can also constrain action maps through its diffuse connections with the dorsal visual stream, known to be involved in the perception of emotional expressions(Engelen et al, 2015(Engelen et al, , 2018, and the translation into action opportunities, in connection with the premotor cortex(Cisek, 2007;Orban, Lanzilotto, et al, 2021;Orban, Sepe, et al, 2021;Rizzolatti et al, 2014). For instance, and in line with monkey studies, it has recently been shown that intraparietal and premotor regions, as well as the AMY, respond to approaching threatening individuals that are about to invade our peripersonal space, in order to rapidly prepare defensive actions (de Borst & de Gelder, 2022).6 -License CC BY…”