Research reportSeeing fearful body language rapidly freezes the observer's motor cortex
Introduction
Different lines of evidence suggest that threat-related signals are rapidly and efficiently processed in the central nervous system (Adolphs and Tranel, 2003, LeDoux, 1996, Öhman and Mineka, 2001) and that attention tends to be prioritized towards threatening stimuli (Fox et al., 2000, Vuilleumier, 2002).
Fearful body language is a salient emotional signal, easily observable from a distance that alerts the observer to the presence of a potential threat (de Gelder et al., 2004, Tamietto et al., 2007). Perceiving fearful expressions in others requires specific processing in an attempt to garner more information about the source of the threat in the surrounding environment (Whalen et al., 1998). Indeed, behavioral studies have shown enhanced sensory acquisition (Lee, Susskind, & Anderson, 2013), perceptual processing (Phelps, Ling, & Carrasco, 2006) and attention (Davis and Whalen, 2001, Kret et al., 2013) when exposed to fearful expressions. Notably, electrophysiological studies have also reported a rapid bias in visual attention allocation with greater resources devoted to fearful expressions; they reported increased amplitudes or shorter latencies of early (100–200 msec) occipito-temporal event-related potential (ERP) components when viewing fearful body expressions (Jessen and Kotz, 2011, Van Heijnsbergen et al., 2007) and facial expressions (Pourtois et al., 2005, Righart and de Gelder, 2006, Williams et al., 2006) relative to emotionally positive and neutral expressions.
Besides increasing sensory vigilance for monitoring potential threats, the sight of fearful expressions may affect the motor system. Animal research has shown that initial reactions to sudden stimuli - and potential threats, in particular - involve reducing motor output, i.e., implementing freezing behavior or orienting immobility while monitoring the source of danger (Fanselow, 1994; Hagenaars, Oitzl, & Roelofs, 2014). Similar phenomena have been suggested in humans (Fanselow, 1994, Frijda, 2010, Hagenaars et al., 2014, Lang and Bradley, 2010). In keeping with this notion, transcranial magnetic stimulation (TMS) studies have documented fast reductions in motor excitability following salient and potentially noxious stimuli like strong, unexpected or rapidly approaching auditory or visual stimuli (Avenanti et al., 2012, Cantello et al., 2000, Furubayashi et al., 2000, Makin et al., 2009, Serino et al., 2009), and painful stimuli self-experienced (Farina et al., 2003, Farina et al., 2001, Urban et al., 2004) or observed in others (Avenanti et al., 2006, Avenanti, Minio-Paluello, Bufalari, et al., 2009a, Avenanti, Minio-Paluello, Sforza, et al., 2009b). Moreover, a reduction of activity in primary motor cortex (M1) has been reported during periods in which participants expect to receive painful stimuli relative to conditions without pain expectation (Butler et al., 2007).
Remarkably, imaging studies have shown that observing fearful expressions in others activates subcortical (e.g., amygdala, superior colliculus) and cortical regions (e.g., cingulate cortex and supplementary motor area, SMA) known to be involved in emotional processing and motor control (de Gelder et al., 2004, de Gelder et al., 2010, Grèzes et al., 2007, Hadjikhani and de Gelder, 2003, Kret et al., 2011, Thielscher and Pessoa, 2007, Vuilleumier et al., 2001, Vuilleumier and Pourtois, 2007). However, the nature of such activations is ambiguous because imaging can hardly distinguish between motor inhibition (which would support freezing-like body immobilizations) and excitation (which would reflect increased action readiness) and cannot precisely determine when these modulations occur. On the other hand, the high temporal resolution of TMS and its ability to distinguish between excitatory and inhibitory activity in motor areas allow effective exploration of motor dynamics during emotion perception.
The goal of this study was to test whether exposure to fearful body postures rapidly reduces excitability in the observer's M1. To this aim, we used TMS over M1 to non-invasively assess motor excitability during perception of emotional body expressions. In previous studies, we started to investigate the dynamics of the human motor system by assessing corticospinal excitability in the observers' left and right M1 during an emotion recognition task (Borgomaneri et al., 2012, Borgomaneri et al., 2014b). We recorded motor-evoked potentials (MEPs) at 150 and 300 msec after the presentation of fearful, happy and neutral expressions in which the body posture was presented in isolation, with no contextual or facial cues. In the earlier time window (150 msec) we found a weak increase in corticospinal excitability in the left hemisphere in response to fearful body postures, suggesting action preparation activity in the motor representation of the dominant hand (see also Borgomaneri et al., 2013, Schutter et al., 2008 for similar findings using fearful facial expressions and negative natural complex scenes). Remarkably, in the same time window, we found a consistent reduction of corticospinal excitability in the right hemisphere for both fearful and happy body postures (Borgomaneri et al., 2014b). This reduction in motor excitability also appeared to be causally related to visual recognition of body postures. TMS over right M1 (but not left M1) at 150 msec after visual stimulus onset also decreased the ability to recognize the observed body postures. The decrease in performance additionally correlated with the reduction in corticospinal excitability, suggesting a close link between motor suppression in the right M1 and perceptual processing of body postures.
At the later stage (300 msec), greater MEP amplitudes were measured when viewing fearful, happy and emotionally neutral dynamic body postures relative to emotionally neutral static body postures. This later increase in motor excitability was similar in the two hemispheres. Moreover, it was comparable for the three dynamic postures (see also Borgomaneri et al., 2012) and likely reflected motor resonance, i.e., the embodiment of the actor's movements into one's own motor system (Bastiaansen et al., 2009, Gallese et al., 2004, Gallese and Sinigaglia, 2011, Keysers and Gazzola, 2009, Niedenthal et al., 2010, Oberman et al., 2007, Rizzolatti and Sinigaglia, 2010) that is typically detected in similar time windows (200–400 msec) according to TMS and MEG evidence (Barchiesi and Cattaneo, 2013, Cavallo et al., 2014, Naish et al., 2014, Nishitani et al., 2004). Consistent with this interpretation, the magnitude of the later motor facilitation also correlated with dispositional cognitive empathy scores (Borgomaneri et al., 2014b), as previously shown in a number of studies investigating motor resonance (e.g., Avenanti, Minio-Paluello, Sforza, et al., 2009b, Avenanti et al., 2010, Gazzola et al., 2006, Lepage et al., 2010, Minio-Paluello et al., 2009). In contrast to the effect reported at 150 msec, neither stimulation of the right nor the left M1 at 300 msec affected visual recognition of body postures. These findings indicated that, at this stage of processing (300 msec), neural activity reflecting motor resonance was stronger in highly empathetic participants who tend to take the psychological perspectives of others in daily life, but was not critical for visual recognition of emotional body postures. These results revealed two distinct functional stages of motor cortex involvement during perception of emotional body language: an initial stage (∼150 msec) reflecting increased motor readiness in the left hemisphere and perceptual mechanisms in the right hemisphere, and a later stage (∼300 msec) in which the motor cortices bilaterally implement motor resonance, which may reflect a more sophisticated and empathy-related reading of the observed body expression “from the inside” (Avenanti, Candidi, et al., 2013b, Avenanti and Urgesi, 2011, Gazzola et al., 2006, Rizzolatti and Sinigaglia, 2010).
In the present study, we sought to further investigate motor responses to emotional bodies in the right and left hemispheres and to test the possible existence of an earlier additional stage of M1 involvement during perception of emotional bodies. Our previous studies suggested comparable motor reactivity in response to happy and fearful body expressions when motor excitability was tested in the 150–300 msec temporal window after visual stimulus onset (Borgomaneri et al., 2012, Borgomaneri et al., 2014b). Here, based on the evolutionary contentions that i) emotional and, in particular, threat-related stimuli should evoke extremely rapid motor reactions (Carretié et al., 2001, Costa et al., 2013, Frijda, 2009, Lang et al., 2000, Öhman and Mineka, 2001); and ii) fear-related signals might reduce motor readiness (as in orienting immobility and freezing responses) to allow environmental monitoring for the source of danger (Fanselow, 1994, Frijda, 2010, Hagenaars et al., 2014, Lang and Bradley, 2010, Whalen et al., 1998), we tested the hypothesis that a transient suppression of motor reactivity would be detected at a very early time window when viewing fearful bodies. To this aim, we investigated motor excitability in the right and left M1 within the same temporal window in which fearful faces and bodies are known to induce the earliest modulation of occipito-temporal cortices (i.e., at 100–125 msec, corresponding to the timing of the P1 component; Pourtois et al., 2005, Righart and de Gelder, 2006, Van Heijnsbergen et al., 2007, Vuilleumier and Pourtois, 2007, Williams et al., 2006).
Similarly to previous research on emotion perception, we used single-pulse TMS over M1 in order to record MEPs from the hand muscles and thus assess how visual perception affects the functional state of the observer's corticospinal system. However, it should be noted that the MEP amplitude obtained with single-pulse TMS reflects the net effect of excitatory and inhibitory inputs to the corticospinal pathway, providing a measure of both cortical and spinal excitability (Di Lazzaro et al., 2001). To directly assess modulations of intracortical excitability within the right and left M1, in the present study, we used for the first time in emotion perception research the paired-pulse protocol, in which pairs of TMS stimuli are administered through a single coil placed over the target M1. In paired-pulse TMS, a conditioning stimulus (CS) below the threshold intensity needed to elicit a MEP is followed at short interstimulus intervals (ISIs) by a suprathreshold test stimulus (TS). At ISIs of 1–5 msec, the CS results in MEP inhibition (i.e., “short intracortical inhibition”, SICI), while longer ISIs of 7–20 msec produce MEP facilitation (“intracortical facilitation”, ICF). This modulation of MEP size takes place at the cortical level and is thought to reflect the activation of separate populations of inhibitory and excitatory cortical interneurons without affecting spinal circuits (Kujirai et al., 1993). In particular it is held that SICI and ICF mainly reflect the activation of low threshold inhibitory interneurons mediated by gamma-aminobutyric acid (GABA) (Di Lazzaro et al., 2000, Ilić et al., 2002, Ziemann et al., 1996aa) and glutamatergic interneurons (Nakamura et al., 1997, Ziemann, 2003), respectively. Therefore, paired-pulse TMS provides reliable indices of motor cortical activations. Here, taking advantage of these paired-pulse paradigms, we aimed to further investigate whether the excitatory or inhibitory intracortical neural circuits within the right and left M1 are modulated during observation of emotional body expressions. By comparing neurophysiological indices of intracortical and corticospinal excitability, we tested whether the sight of emotional bodies at an early time window (100–125 msec) affected the observers' M1, descending corticospinal pathways or both. This allowed us to demonstrate that, before perceptual- and action-related processing at 150 and 300 msec (see Borgomaneri et al., 2012, Borgomaneri et al., 2014b), the motor system in both hemispheres implements fast suppression of motor reactions to emotional bodies with stronger suppression for fearful body expressions.
Section snippets
Participants
Twenty-eight healthy subjects took part in the study. Fourteen participants (6 men, mean age ± S.D.: 22.8 y ± 2.6) were tested in a first experiment in which the right M1 was stimulated (Exp1M1right), whereas the remaining 14 participants (7 men, mean age ± S.D.: 23.3 y ± 2.6) were tested in a second experiment in which the left M1 was stimulated (Exp2M1left). All participants were right-handed according to a standard handedness inventory (Oldfield, 1971) and free from any contraindication to
Subjective measures
Mean task accuracy in the three sessions was high in both experiments (Exp1M1right: SP mean accuracy ± S.D.: 90.7% ± 5.3; SICI: 89.5% ± 6.7 and ICF: 90.5% ± 5.3; Exp2M1left: SP mean accuracy ± S.D.: 92.7% ± 5.5; SICI: 91.7% ± 5.2 and ICF: 90.6% ± 4.9). The Experiment × Session ANOVA carried out on accuracy data showed no main effects or interactions (all F < .95; p > .39), suggesting similar accuracy across the two experiments and three TMS sessions.
The Experiment × Movement type ANOVAs carried
Discussion
Emotional body language represents a powerful vehicle for interpersonal communication (Darwin, 1872), and it is widely assumed that processing emotional language can prime the body for action (Ekman and Davidson, 1994, Frijda, 2009, Izard, 1994). However, little is known about how the sight of emotional bodies affects the observer's M1. Using the high temporal resolution of TMS, here, we tested the hypothesis that seeing emotional body expressions – and fearful expressions in particular –
Financial disclosures
Authors have no conflicts of interest to declare.
Acknowledgments
This work was supported by grants from the Cogito Foundation (Research project 2013, R-117/13), Ministero Istruzione, Università e Ricerca (Futuro in Ricerca 2012, RBFR12F0BD) and Ministero della Salute (Bando Ricerca Finalizzata Giovani Ricercatori 2010, GR-2010-2319335) awarded to A.A. and a VENI grant (451-09-006) from the Netherlands Organization for Scientific Research (N.W.O.) to V.G.
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2022, Current Research in Behavioral SciencesCitation Excerpt :The notion that seeing expressive whole-body postures and movements triggers motor preparation was at the core of the earliest studies on body expressions (e.g., de Gelder et al., 2004) but no direct physiological or behavioral evidence was so far available. Consistent with this perspective, Borgomaneri and colleagues (2015) showed that watching fearful body expressions suppresses TMS-induced intracortical facilitation in the motor cortex and the authors interpreted this as an index of freezing response when observing a cue indicating a potential threat in the environment. We expand this at the behavioral and physiological levels by showing that facing an aggressive body posture is also associated with freezing.
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