دانلود مقاله ISI انگلیسی شماره 36874
عنوان فارسی مقاله

مشاهده زبان بدن هراسان سریعا قشر حرکتی ناظر را مسدود می کند

کد مقاله سال انتشار مقاله انگلیسی ترجمه فارسی تعداد کلمات
36874 2015 14 صفحه PDF سفارش دهید 7880 کلمه
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عنوان انگلیسی
Seeing fearful body language rapidly freezes the observer's motor cortex
منبع

Publisher : Elsevier - Science Direct (الزویر - ساینس دایرکت)

Journal : Cortex, Volume 65, April 2015, Pages 232–245

کلمات کلیدی
بدن عاطفی - پردازش ترس - انجماد - قشر حرکتی - تسهیل - تحریک مغناطیسی ترانس کرانیال
پیش نمایش مقاله
پیش نمایش مقاله مشاهده زبان بدن هراسان سریعا قشر حرکتی ناظر را مسدود می کند

چکیده انگلیسی

Fearful body language is a salient signal alerting the observer to the presence of a potential threat in the surrounding environment. Although detecting potential threats may trigger an immediate reduction of motor output in animals (i.e., freezing behavior), it is unclear at what point in time similar reductions occur in the human motor cortex and whether they originate from excitatory or inhibitory processes. Using single-pulse and paired-pulse transcranial magnetic stimulation (TMS), here we tested the hypothesis that the observer's motor cortex implements extremely fast suppression of motor readiness when seeing emotional bodies – and fearful body expressions in particular. Participants observed pictures of body postures and categorized them as happy, fearful or neutral while receiving TMS over the right or left motor cortex at 100–125 msec after picture onset. In three different sessions, we assessed corticospinal excitability, short intracortical inhibition (SICI) and intracortical facilitation (ICF). Independently of the stimulated hemisphere and the time of the stimulation, watching fearful bodies suppressed ICF relative to happy and neutral body expressions. Moreover, happy expressions reduced ICF relative to neutral actions. No changes in corticospinal excitability or SICI were found during the task. These findings show extremely rapid bilateral modulation of the motor cortices when seeing emotional bodies, with stronger suppression of motor readiness when seeing fearful bodies. Our results provide neurophysiological support for the evolutionary notions that emotion perception is inherently linked to action systems and that fear-related cues induce an urgent mobilization of motor reactions.

مقدمه انگلیسی

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 and Öhman and Mineka, 2001) and that attention tends to be prioritized towards threatening stimuli (Fox et al., 2000 and 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 and 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 and 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 and Van Heijnsbergen et al., 2007) and facial expressions (Pourtois et al., 2005, Righart and de Gelder, 2006 and 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 and 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 and Serino et al., 2009), and painful stimuli self-experienced (Farina et al., 2003, Farina et al., 2001 and Urban et al., 2004) or observed in others (Avenanti et al., 2006, Avenanti, Minio-Paluello, Bufalari, et al., 2009a and 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 and 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 and 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 and 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 and 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 and 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 and 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 and 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 and 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 and 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 and 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 and 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 and Ziemann et al., 1996aa) and glutamatergic interneurons ( Nakamura et al., 1997 and 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 and 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.

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