Early changes in corticospinal excitability when seeing fearful body expressions.

Sara Borgomaneri,Alessio Avenanti,Francesca Vitale

doi:10.1038/srep14122

Abstract

Quick inhibition of approach tendencies in response to signals of potential threats is thought to promote survival. However, little is known about the effect of viewing fearful expressions on the early dynamics of the human motor system. We used the high temporal resolution of single-pulse and paired-pulse transcranial magnetic stimulation (TMS) over the motor cortex to assess corticospinal excitability (CSE) and intracortical facilitation (ICF) during observation of happy, fearful and neutral body postures. To test motor circuits involved in approach tendencies, CSE and ICF were recorded from the first dorsal interosseous (FDI), a muscle involved in grasping, and the abductor pollicis brevis (APB), which served as a control. To test early motor dynamics, CSE and ICF were measured 70–90 ms after stimulus onset. We found a selective reduction in CSE in the FDI when participants observed fearful body expressions. No changes in ICF or in the excitability of APB were detected. Our study establishes an extremely rapid motor system reaction to observed fearful body expressions. This motor modulation involves corticospinal downstream projections but not cortical excitatory mechanisms, and appears to reflect an inhibition of hand grasping. Our results suggest a fast visuo-motor route that may rapidly inhibit inappropriate approaching actions.

Highlights

Testing motor excitability in this temporal window is interesting because this window: i) corresponds to the peak latency of the earliest cortical response to visual stimuli in the primary visual cortex, i.e., the C1 event-related potential (ERP) component[31], and C1 amplitude was modulated by fearful facial expressions in previous research[6,32]; ii) represents a phase in which visual stimuli are not fully processed at a conscious level, according to current models of object recognition and visual consciousness[33,34]
We assessed changes in corticospinal excitability (CSE) induced by the observation of emotional body postures by using single-pulse TMS to elicit motor-evoked potentials (MEPs) from the first dorsal interosseous (FDI) and abductor pollicis brevis (APB) muscles
MEP amplitudes in the single-pulse session were analyzed by means of a three-way repeated-measures ANOVA with the factors Muscle (2 levels: FDI and APB), Time (2 levels: 70 and 90 ms) and Posture (3 levels: happy, fearful and neutral)

Summary

Introduction

The SICI and ICF indices are thought to reflect the activation of separate populations of inhibitory GABAergic and excitatory glutamatergic cortical interneurons in M1, respectively, and provide reliable measures of motor cortical activations[20,21] Using such TMS protocols, we have recently tested whether observing fearful body expressions rapidly affects the motor system[22,23,24]. Testing motor excitability in this temporal window is interesting because this window: i) corresponds to the peak latency of the earliest cortical response to visual stimuli in the primary visual cortex, i.e., the C1 ERP component[31], and C1 amplitude was modulated by fearful facial expressions in previous research[6,32]; ii) represents a phase in which visual stimuli are not fully processed at a conscious level, according to current models of object recognition and visual consciousness[33,34] This design may provide insights into the rapid and unconscious processing of emotions.

Methods

Results

Conclusion