The human ability to perceive and understand others actions, emotions, and intentions is pivotal to the formation of social interactions, communication, and relationships. At the neural level, studies have revealed a set of brain regions which are part of the action perception network or mirror system and which are particularly involved in human motion perception (Gallese et al., 2004; Rizzolatti and Craighero, 2004; Rizzolatti and Fabbri-Destro, 2008). The existence of “mirror” neurons was first described in the macaque monkey brain using single-cell recordings (di Pellegrino et al., 1992). Later, neuroimaging and neurophysiological research confirmed the existence of a similar “fronto-parietal” mirror system in the human brain (Fadiga et al., 1995; Grafton et al., 1996; Iacoboni et al., 1999). In addition to the mirror-motor areas in the inferior parietal, inferior frontal gyrus and premotor cortex, the action perception network also encompasses higher-order visual areas in the posterior superior temporal sulcus (pSTS) that convey visual input to downstream visuo-motor areas (Rizzolatti and Craighero, 2004; Caspers et al., 2010; Molenberghs et al., 2010, 2012). Especially the right pSTS has been highlighted as a key neural locus for perception of bodies and biological motion (Allison et al., 2000), as it has been shown to be particularly activated during the perception of eye or mouth movements, body language, and biological motion (Allison et al., 2000; Hein and Knight, 2008; Redcay, 2008; Carrington and Bailey, 2009).

Prior research most frequently adopted the so-called point-light displays (PLDs) to study the neural basis of biological movement perception as they represent a highly controllable, impoverished form of biological motion (Johansson, 1973). In these displays, only a few bright moving point-light dots are depicted against a dark background to represent the movement of the main joints of a human body. Although they lack any information on texture or form, PLDs are highly salient in depicting human actions as well as information on the gender or emotional state in which the point-light figure is engaged (Johansson, 1973; Cutting and Kozlowski, 1977; Dittrich et al., 1996; Pollick et al., 2002, 2005; Alaerts et al., 2011).

To date, two studies investigated the causal relationship between the ability to perceive PLDs and intact functioning of the (right) pSTS (Grossman et al., 2005; van Kemenade et al., 2012). In these studies, repetitive transcranial magnetic stimulation (rTMS) was used to temporarily disrupt activity in right pSTS and both reported deteriorated performance on a task involving the detection of biological motion in noise-masked displays (Grossman et al., 2005; van Kemenade et al., 2012).

Here, we used a transcranial direct current stimulation (tDCS) paradigm to investigate whether neural information processing can be up- or down-regulated in order to increase or deteriorate biological motion perception. Development of brain stimulation paradigms that can enhance biological motion perception abilities would be of particular interest for neuropsychiatric conditions that have clear implications in social and communicative domains, such as autism spectrum disorders (ASD). At the behavioral level, ASD-related deficiencies in biological motion perception have been reported repeatedly (Kaiser and Pelphrey, 2012) and also previous neuroimaging studies from our and other labs showed altered activity and connectivity patterns in pSTS regions in the autistic brain (Freitag et al., 1994; Pelphrey et al., 2011; Alaerts et al., 2014). Particularly tasks including an emotion processing component (e.g., reporting the emotional state of PLD figures) have shown highly consistent ASD-specific deficiencies (Hubert et al., 2007; Parron et al., 2008; Atkinson, 2009; Nackaerts et al., 2012; Alaerts et al., 2014).

In the present study, we applied tDCS with anodal (excitatory) or cathodal (inhibitory) electrodes mounted over right pSTS (target) and orbito-frontal cortex (reference) in healthy human subjects while they performed a bodily emotion recognition task using PLDs. Performance [accuracy and reaction times (RTs)] was also assessed on a control task that was matched to the emotion recognition task in terms of cognitive and motor demands. Each subject participated in two experimental sessions, receiving either anodal or cathodal stimulation, separated by one week to avoid residual effects of previous stimulations. Based on previous studies and in the light of our anatomical hypothesis, we expected anodal (excitatory) stimulation over right pSTS to increase sensitivity to biological motion thereby enhancing emotion recognition abilities. Cathodal (inhibitory) tDCS over pSTS is expected to reduce or have no effect on performance.

In this study, we investigated the role of the posterior superior temporal sulcus (pSTS) in emotion recognition from PLDs. To do so, tDCS was applied using anodal (excitatory) or cathodal (inhibitory) electrodes mounted over right pSTS (target) and orbito-frontal cortex (reference) in two separate sessions. Half of the subjects received anodal stimulation over pSTS on the first session, the other half started with cathodal stimulation over pSTS with at least one week in-between.

Based on our primary analysis, we found no evidence that general emotion recognition from PLDs was affected by receiving anodal or cathodal stimulation over pSTS. However, exploratory analyses provided indications that effects of stimulation were dependent on the emotional valence of the presented stimuli. Particularly, when effects of stimulation were explored separately for emotion categories with a “negative” (sadness–anger) or “positive–neutral” (happy, neutral) emotional valence, it was revealed that performance scores for recognizing emotional states with a negative emotional valence significantly increased from receiving anodal (excitatory) stimulation compared to cathodal (inhibitory) stimulation over pSTS, whereas no stimulation effects were shown for recognizing emotional states with a positive–neutral emotional valence. No effects of stimulation were revealed for performance on the control task. Although effects are preliminary, these results provide first indications that tDCS stimulation over pSTS can modulate (negative) bodily emotion recognition from PLDs.

While anodal/cathodal tDCS was targeted over the pSTS, reference electrodes were placed over left orbito-frontal cortex. Similar supra-orbital reference placements have been adopted previously in studies from our (Zhang et al., 2014) and other (Nitsche and Paulus, 2000) labs targeting primary motor cortex to constrain stimulation effects to frontal areas. In our study, it is likely that tDCS affected excitability in orbito-frontal and prefrontal cortex, thereby modulating excitability in a large fronto-temporal network, potentially overlapping with the mentalizing network or social brain [e.g., Allison et al. (2000)]. In depressed patients, excitability-enhancing tDCS over dorso-lateral prefrontal cortex has been shown to improve performance in an affective go-no-go task for positive emotional content (Boggio et al., 2007). Also in healthy participants, prefrontal tDCS has been shown to diminish emotional valence of unpleasant pictures (Boggio et al., 2009; Maeoka et al., 2012) or subtly improve emotional face identification (Nitsche et al., 2012) [but see Plazier et al. (2012)]. Future experiments are warranted to formally assess whether reference electrode placement to areas other than orbito-frontal sites may qualitatively alter the reported effects. Also other procedures can be adopted to increase focality and stimulation efficacy to the targeted region, such as high-definition tDCS using a 4 × 1 electrode placement (constraining current flow to a circumscribed area of four reference electrodes surrounding the target electrode).

To our knowledge, this is the first study to explore the effects of anodal/cathodal tDCS over the posterior STS. In the past, two studies have applied rTMS over the pSTS region during perception of PLDs. In one study, Grossman et al. (2005) applied rTMS over right pSTS and subsequently measured sensitivity to biological motion. The task required subjects to recognize canonical (upright) point-light animations and 180° inverted animations. Here, rTMS resulted in a decreased sensitivity for recognizing upright biological motions, but stimulation did not affect performances for recognizing the inverted animations (Grossman et al., 2005). In another study by van Kemenade et al. (2012), TMS was applied over the left pSTS, the ventral premotor cortex and the vertex (control site). The task involved the recognition of PLDs of human animations masked in noise from scrambled versions of the same stimuli and performances were measured before and after 20 s of continuous theta burst stimulation of premotor, pSTS, and the control site (each tested on different days). Here, authors reported a significant decrease in detection of human PLDs when disrupting the premotor cortex and a marginally significant decrease in detection when left pSTS was stimulated (van Kemenade et al., 2012).

While Grossman et al. (2005) and van Kemenade et al. (2012) used PLDs to assess effects of rTMS over pSTS, other studies used different task paradigms to assess the role of STS in emotion or motion processing. For example, Pitcher (2014) measured the effects of rTMS over right STS during the recognition of facial emotional expressions and found that repetitive TMS specifically deteriorated performance on the facial emotion recognition task, not on a matched control task requiring the identification of faces. Another study applied rTMS over left STS during action observation, and showed that the “mapping” of observed “implied” actions onto the observer’s motor system (as measured by changes in cortico-motor excitability in primary motor cortex) was enhanced from stimulating left STS (Avenanti et al., 2013).

More recently, Arfeller et al. (2013) used fMRI to explore changes in the functional connections of left and right pSTS after application of rTMS. Interestingly, brain regions showing changes were identified in lateral temporo-occipital cortex, the anterior intraparietal region and in the ventral premotor cortex. Considering that these are all regions of the action perception or “mirror” network, the authors concluded that STS plays a pivotal relay position during the observation of others movements (Arfeller et al., 2013). This notion conforms to findings from an earlier lesion study showing that lesions in superior temporal and premotor areas have causal relationships to deficits in biological motion perception (Saygin, 2007).

In the present study, tDCS stimulation mildly affected emotion recognition from PLDs, at least for emotional states with a “negative” emotional valence. One study similarly showed that tDCS over the cerebellum specifically affected recognition of negative facial emotions (anger, sadness), not of positive or neutral faces (Ferrucci et al., 2012). A selective effect for negative emotional stimuli was also reported in a study by Candidi et al. (2011), showing that rTMS over right pSTS specifically deteriorated the detection of threatening human body postures, not the detection of neutral postures (Candidi et al., 2011). Also repetitive TMS over the frontal sensorimotor system specifically interfered with the recognition of faces expressing anger and fear, not happy or neutral faces (Balconi and Bortolotti, 2012). Several studies on emotional face processes indicated that distinct emotions may be processed differently. For example, by using the “face-in-the-crowd” paradigm, Ohman et al. (2001) showed that among faces expressing various emotions, a face expressing anger was processed faster and more accurately than other facial expressions (Ohman et al., 2001). Also for PLDs, an increase in visual sensitivity has been demonstrated for detecting angry walkers (Chouchourelou et al., 2006). Another study showed that the detection of human gait in PLD biological motion correlated with the detection of angry point-light figures, but not happy figures (Ikeda and Watanabe, 2009). It has been proposed that threatening stimuli may be processed more automatically thereby explaining the higher sensitivity to anger in these previous studies. Specifically, the “threat advantage hypothesis” suggests that natural selection resulted in a propensity to react more strongly and automatically to negative than to positive stimuli (Fox et al., 2000). In relation to our study, it can be speculated that tDCS over right pSTS predominantly affected the automatic processing of emotional states, hence the specificity for emotional states with negative emotional valence. However, considering that the present experiment was not a priori designed to disentangle the differential effect of stimulation on processing negative/positive–neutral emotional states (limited number of trials for each emotion category), future studies, specifically testing stimulation effects on distinct emotion categories, are warranted to be conclusive on this interpretation.

In our experiment, only the right, not the left pSTS, area was disrupted or stimulated. The suggestion of right hemisphere specialization for processing facial or other non-verbal social cues knows a long history and is based on several clinical observations and neuroimaging studies (Fusar-Poli et al., 2009). Also a very recent study confirmed the notion of right lateralization for perceiving emotional dynamic faces in human pSTS (De Winter et al., 2015). Nevertheless, compensatory contributions of left pSTS or other fronto-parietal regions (e.g., premotor cortex) cannot be ruled out. For example, one study, examining effects of rTMS stimulation over left and right superior temporal lobe, showed that stimulation over both hemispheres can increase attention selectively for angry faces (not for fearful or neutral faces) (Brüne et al., 2006). The latter study therefore indicates that not only right but also left pSTS may play an important role in directing and processing of negative emotional states such as anger. Interestingly, the study by Brüne et al. additionally showed that right hemisphere stimulation more strongly affected processing of male angry faces, whereas right hemisphere stimulation more strongly affected processing of female angry faces. Although preliminary, the authors suggested that this hemispheric specialization might reflect a divergent significance for processing male and female threat (Brüne et al., 2006).

One limitation of this study is the lack of a sham condition (during which no stimulation is applied). Future research is therefore necessary to firmly disentangle whether anodal/cathodal stimulation increased/decreased performance compared to baseline for detecting emotional states with negative emotional valence. Also for the emotion conditions and control task where stimulation showed no effects on performance, a baseline condition is necessary to formally exclude the possibility that anodal and cathodal produced a uniform effect on performance (e.g., both increasing or deteriorating performance). Indeed, in a recent study examining effects of anodal and cathodal tDCS over left primary motor cortex, it was shown that anodal and cathodal tDCS, when applied at similar intensities and duration, can produce similar changes in cortico-motor excitability (Batsikadze et al., 2013).

In summary, the present study found no overall effect of tDCS brain stimulation on bodily emotion recognition from PLDs. However, when emotion categories were explored separately, a significant effect of stimulation was revealed for recognizing emotional states with a negative emotional valence (sadness and anger), as indicated by higher performance during anodal (excitatory) stimulation, compared to cathodal (inhibitory) stimulation over pSTS. This finding partly agrees with previous studies showing structure–function relationships between STS and biological motion processing from PLDs and provides indications that stimulation effects may be modulated by the emotional valence of the stimuli.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The Supplementary Material for this article can be found online at http://journal.frontiersin.org/article/10.3389/fnhum.2015.00438