Abstract Recent event-related potential studies have shown that the occipitotemporal N170 component - best known for its sensitivity to faces - is also sensitive to perception of human bodies. Considering that in the timescale of evolution clothing is a relatively new invention that hides the bodily features relevant for sexual selection and arousal, we investigated whether the early N170 brain response would be enhanced to nude over clothed bodies. In two experiments, we measured N170 responses to nude bodies, bodies wearing swimsuits, clothed bodies, faces, and control stimuli (cars). We found that the N170 amplitude was larger to opposite and same-sex nude vs. clothed bodies. Moreover, the N170 amplitude increased linearly as the amount of clothing decreased from full clothing via swimsuits to nude bodies. Strikingly, the N170 response to nude bodies was even greater than that to faces, and the N170 amplitude to bodies was independent of whether the face of the bodies was visible or not. All human stimuli evoked greater N170 responses than did the control stimulus. Autonomic measurements and self-evaluations showed that nude bodies were affectively more arousing compared to the other stimulus categories. We conclude that the early visual processing of human bodies is sensitive to the visibility of the sex-related features of human bodies and that the visual processing of other people's nude bodies is enhanced in the brain. This enhancement is likely to reflect affective arousal elicited by nude bodies. Such facilitated visual processing of other people's nude bodies is possibly beneficial in identifying potential mating partners and competitors, and for triggering sexual behavior.

Citation: Hietanen JK, Nummenmaa L (2011) The Naked Truth: The Face and Body Sensitive N170 Response Is Enhanced for Nude Bodies. PLoS ONE 6(11): e24408. https://doi.org/10.1371/journal.pone.0024408 Editor: Hans P. Op de Beeck, University of Leuven, Belgium Received: February 17, 2011; Accepted: August 10, 2011; Published: November 16, 2011 Copyright: © 2011 Hietanen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Academy of Finland grants #130272 to J.K.H and #121031 to L.N. and the AivoAALTO Grant from the Aalto University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction Without any doubt, other human beings are the most important visual objects in our environment. Compatible with this, cognitive neuroscience has revealed that the perception of other human beings is based on brain mechanisms specifically devoted to processing visual information from this socially and biologically relevant class of stimuli [1]. Much research has focused on neurocognitive mechanisms subserving perception of human faces and bodies as they both provide information necessary for social interaction and interpersonal relationships. Several lines of evidence suggest that both human and sub-human primate brains contain cells specialized in processing of facial information [2]–[4]. For example, functional neuroimaging studies have identified an interconnected occipitotemporal neural network which shows face-selective response properties and high level of specialization in processing of the facial image [3], [5], [6]. Perception of human bodies is also subserved by a specialized brain network [7]–[9]. Paralleling the functional properties of the face-sensitive mechanisms, these lateral and ventral occipito-temporal circuits are engaged more vigorously during the perception of human bodies and body parts than during the perception of inanimate objects, isolated body parts or faces [7], [10], [11]. Electroencephalography (EEG) and magnetoencephalography (MEG) studies have investigated the early stages of visual processing of human faces and bodies. These studies have identified an event-related potential (ERP) and its magnetic counterpart recorded over occipito-temporal regions peaking between 140–200 ms after stimulus onset and being more sensitive to faces than to other objects [12]–[15]. Because of the typical peak latency (170 ms) of this negative potential, it is often referred to as N170 response. However, whether the N170 reflects only processes related to face perception is still a matter of great debate [14], [16], [17]. It has indeed been shown that the perception of bodies also triggers a profound N170 component whose amplitude is greater than that triggered by objects, but smaller than [18], [19] or similar [20], [21] to that triggered by faces. The body-sensitivity of the N170 response could be explained by arguing that the N170 response reflects the processing of configurally represented information [22] which is important both for face [23] and body [24] perception. Compatible with this view, the N170 response to both faces and bodies shows response characteristics considered typical for configural or holistic processing of visual stimuli, such as sensitivity to spatial inversion of stimuli [19], [25]–[27]. However, considering that the potential distribution and source localization of the N170 response differ between bodies and faces [18], [20], it is reasonable to assume that the N170 response does not reflect mere general configural processing of visual objects. More likely, it is driven by activation of the above-mentioned occipito-temporal areas specialized for processing of faces and bodies. In all the aforementioned electrophysiological studies investigating the early visual processing of body information [18]–[21], [26], [27], the bodies were presented as wearing clothes. However, during the evolution, the cortical networks specialized in body perception have probably been tuned to respond to nude bodies. Although clothing provides cues to gender, sexual status, and rank in many cultures, clothing is typically used to restrict the visibility of the body, especially the primary and secondary sexual cues, and thus clothing hides bodily features relevant for sexual selection and arousal. Among primates, identification of mating partners relies extensively on the visual system [28] and humans, like other primates, display highly selective preferences in viewing the sexual signals of conspecifics [29], [30]. Perception of these signals and their evaluation as positive leads to physiological arousal, which can subsequently trigger sexual behaviors and ultimately copulation [31]. Efficient perception of sexual signals and categorization of conspecifics as potential mating partners or competitors is thus essential for both sexual selection and ensuring reproduction in primates. Earliest recorded signs of clothing date to 36,000 BCE [32], although genetic and molecular clock estimates of the head and body lice – the latter having little chance of surviving on naked human body – suggest that body lice have originated already 72,000±42,000 years ago, which could coincide with the beginning of frequent use of clothing [33]. Thus, considering that the use of clothing has a relatively short history in the time-scale of evolution, it is possible that the responses of the brain networks specialized in body perception could show attenuated responses towards bodies wearing clothing. It has actually been proposed that colour vision might have evolved in primates for discriminating the spectral modulations on the skin of conspecifics [34]. In line with this, human visual system has been found to be particularly sensitive to detecting desaturated reddish targets resembling human skin tones [35]. Against this background, an interesting question arises: does the human brain show enhanced visual processing of nude over clothed bodies, and especially, if so, can we find the enhanced processing already at the early stages of visual processing? As noted, nude bodies, especially of the opposite sex, are affectively pleasant and highly arousing stimuli [36], [37]. There is an extensive literature on affective picture processing showing that stimulus valence and arousal, in general, modulate several ERP components (for a review, see [38]). In this line of research, the high arousing, affectively pleasant stimuli have often included pictures showing nude people. However, none of these studies has investigated specifically the early visual processing of nude bodies. Furthermore, most prior studies have analyzed middle (200–300 ms) or long latency (>300 ms) responses triggered by complex pleasant scenes with varying content. There are, however, also studies that have shown affective modulation on short latency ERP responses. The evidence regarding the affective modulation of the P1 component is inconclusive and, if anything, it suggests that P1 is enhanced to stimuli with unpleasant valence (see [38]). However, reliable affective modulation has been observed for later N1 responses for pleasant [39]–[41] and unpleasant stimuli [40]. There is also some evidence that nude bodies might trigger enhanced early occipitotemporal responses. A MEG study measuring responses specifically to same-sex and opposite-sex nudes reported two early components which were larger to nude bodies than to neutral, non-human objects [42]. The earlier component, with a mean latency of 126 ms, was larger to male and female nudes compared to neutral pictures, but only in male participants, whereas the second component, with a mean latency of 203 ms, was larger to nudes than to neutral pictures in both sexes. However, the responses were averaged over all occipital and temporal channels and, more importantly, responses to nude bodies were compared with those to objects rather than with those to clothed bodies or faces. Thus, these studies do not reveal how nudity influences early visual processing of human bodies. Functional imaging studies with coarser time-scale have also confirmed that occipitotemporal responses are amplified for erotic pictures involving couples as well as single nude bodies (for a review, see Table 1 in [43]). However, due to the limits of temporal resolution of fMRI, these studies have also been unable to characterize the processing in the early visual stages. In sum, although the visual processing of sexually explicit material has been extensively investigated, our knowledge of how clothing affects the early visual responses to human bodies remains elusive. In the present ERP experiments we tested whether the amplitude of the well-known face and body selective N170 component is dependent on whether the bodies were nude or clothed. Because N170 is known specifically for its sensitivity to faces, we also wanted to compare responses to nude and clothed bodies vs. faces. In two experiments we measured ERPs elicited by faces, nude bodies, bodies wearing sexually revealing clothing (swimsuits), fully clothed bodies as well as inanimate control objects (automobiles). Our prediction was straightforward: if the brain prioritizes the visual processing of nude bodies, N170 amplitude should be larger to nude than to clothed human bodies.

Discussion Our ERP data show for the first time that early visual processing of nude over clothed bodies is enhanced. Previous ERP studies had shown that the N170 component is sensitive to perception of human bodies [18]–[21], [26], [27]. The results from the present two experiments showed that the visual processing of male and female human bodies - as reflected by the occipito-temporal N170 response - was enhanced if their sex-related features were visible. Moreover, the results demonstrated that N170 to bodies was sensitive to the degree of sex-related features visible in the bodies: the N170 amplitude increased linearly as the amount of clothing decreased from full clothing via swimsuits to nude bodies. Importantly, our results also showed that the N170 response traditionally assumed to be most pronounced to human faces [12]–[14] turned out to be even greater to nude bodies than to faces. Altogether these results show that early face and body sensitive cortical responses are sensitive to the visibility of the sex-related features of human bodies and that the human brain exhibits enhanced visual processing of other people's nude bodies, a mechanism possibly beneficial in identifying potential mating partners and competitors. But why would the N170 component be sensitive to the degree of nudity of the human bodies? Interpreting our findings against the dominant frameworks of the electrophysiology of face and body perception does not provide a satisfactory explanation. First, assuming that the N170 reflects the engagement of configural processing networks [22] one would have to argue that perception of nude human bodies increasingly activates the neural networks coding configurally or holistically represented visual information. However, this explanation is not very plausible, as our results showed that the nude bodies elicited an even greater N170 response than did human faces, the stimulus category whose perception is considered to be based on a particularly strong configural representation [23]. Second, another prominent hypothesis suggests that the N170 response reflects the functioning of the mechanisms sensitive to extensive experience with any category of visual stimuli (expertise hypothesis [17]). However, in this case, we would have to argue that our participants drawn from the volunteer pool of our university had had more exposure to nude bodies than to clothed bodies and faces. This is not likely, either. A third and a more appealing explanation concerns the role of affective arousal in modulating the amplitude of the N170 response. Our measurements of autonomic responses and self-ratings support for this hypothesis: both measures showed higher arousal to nude bodies than to other stimulus categories, and the overall mean self-reported arousal scores to different stimulus categories were also correlated with the N170 amplitudes. This accords with the extensive literature showing enhanced ERP responses to affectively arousing stimuli (for a review, see [38]). A handful of previous studies has found affective modulation of early visual ERP responses (such as N1, e.g. [39]–[41]. We replicate these findings and show that particularly the face- and body-sensitive occipitotemporal N170 response shows significant sensitivity to a very specific affective signal, namely, the visibility of sex-related human body features. In more general sense the present findings suggest that the face- and body-sensitive N170 response can be greatly modulated by the affective and motivational significance of the stimulus. Previous studies have already shown that the N170 amplitude is enhanced for emotionally arousing faces such as those with fearful rather than neutral facial expressions [57], [58], faces displaying gaze contact rather than gaze aversion (eye contact; [59], [60]), and familiar rather than unfamiliar faces [61]. Interestingly, in previous studies investigating the effects of expressive body postures on early visual processing, N170 has not been found to be modulated by body expressions [26], [62]. However, in one study the VPP (vertex positive potential), a positive counter-part of N170 recorded from the top of the head, was observed to be enhanced to fearful bodies [26]. One possible way to reconcile these seemingly discrepant results is that nude bodies are obviously much stronger and salient affective signals than, for example, fearful body postures. Accordingly, it is understandable that nude bodies but not bodily expressions trigger enhanced N170 amplitudes. Taken together, our results suggest that the N170 component reflects two different types of processes: engagement of visual processing systems specialized for face and body perception, as well as affective-motivational processes tracking emotional arousal level. Configural versus featural processing of visual stimuli has typically been investigated by rotating the stimuli upside down. This manipulation disrupts configural coding and is known to interfere specifically with the perception of faces, bodies, and target objects of expertise. As inversion also increases the latency and sometimes also the amplitude of N170 to these stimuli [25], [26], [63], results from such studies convincingly suggest that N170 reflects visual processing of faces and bodies, and possibly also of other types of configurationally represented visual information. In line with this, we found larger N170 amplitudes for faces vs. cars in the absence of arousal differences between these categories. Accordingly, these differences must be due to an arousal-independent mechanism, such as differential engagement of the category-selective visual processing systems, or those subserving, for example, configural processing of visual information. However, the present data highlight that inputs from brain regions encoding of salient and arousing visual stimuli also contribute significantly to the N170 wave. There is abundant evidence implicating the amygdala as one of the core regions involved in early encoding emotional features from sensory input [64], [65] including sexual cues [66]. It has been proposed [67], [68] that amygdala may accomplish some forms of affective evaluation even before visual information is transmitted to the occipitotemporal areas involved in object recognition. But recently it has been suggested that the cortex may have a more important role in processing of affective information than previously assumed. Pessoa and Adolphs [69] postulated a multiple-waves model emphasizing the existence of multiple parallel cortical routes and several ‘short-cut’ connections between lower and higher visual areas. Such connections would allow affective modulation of short-latency brain responses without a need to rely on subcortical processing. Although we have emphasized the role of affective arousal in generating the enhanced N170 response to nude bodies, there may be other alternatives for explaining the present results. One possibility relates to attentional top-down effects on the N170 responses. Even though many studies have failed to find attention effects on the N170/M170 responses to faces [70]–[72], there are recent studies showing that the N170 response to faces can be sensitive to both spatial [73]–[75] and object-based [76], [77] selective attention. Thus, it is possible that more attention was allocated on nude vs. clothed bodies and the amplitude enhancement of the N170 response may have reflected this effect, at least to some extent. As the effects of affective arousal and attention are tightly intertwined, differentiating between these effects will be an important issue for future studies. Second, based on our results we can not strictly dissociate the contribution of body nudity per se and the contribution of affective arousal on enhanced N170 responses. Disentangling specifically the contribution of affective arousal would have required a control stimulus category not showing body nudity, but associated with positive valence and, importantly, eliciting high arousal comparable to that elicited by nude bodies. However, finding such a stimulus category is not straightforward. Another possibility would be replicating the present experiment with participants such as those with hypoactive sexual disorder, for whom nude bodies are not exceedingly arousing. These patients have, for example, been shown to experience lower level of sexual arousal during viewing of erotic films as compared to controls [78]. Finally, the N170 responses to a face have been shown to decrease when there is another face in the visual field, a finding interpreted to result from competition for recruiting a common population of neurons [79], [80]. Against this finding it is possible that the enhanced N170 response for naked vs. clothed bodies could reflect, in fact, attenuated N170 amplitudes to clothed bodies because of mutual suppressive competition among bodies and object shapes (clothes). In order to test this hypothesis, future studies could investigate, for example, whether presentation of mere clothes next to a nude body results in smaller N170 responses compared to those to the presentation of nude bodies only. An important and yet open question is whether N170 elicited by faces vs. nude and clothed bodies reflects the activation of the same or different neural generators. In previous studies comparing the N170 response between clothed bodies and faces, some researchers have reported similar scalp topography for faces and bodies [26], whereas others have shown that the potential distribution and source localization differ between responses to bodies and faces [18], [20]. The N170 topography of the present study provided evidence for separate sources. However, in the present study the sensor density of 21 electrodes was too low to allow accurate source localization. This question must be addressed in future studies employing high-density electrode networks or magnetoencephalography. It will be of particular interest be to ascertain whether the processing of nude bodies engages only the same cortical sources as the processing of clothed bodies and faces, or whether the N170 response enhancement to nude bodies reflects activation of additional cortical-subcortical generators. Obviously, another great challenge for future research will be to reveal the visual features that make nude human bodies affectively arousing and subject to enhanced visual processing. Conclusions We conclude that the human brain is tuned to detect sexual signals from human bodies rapidly, and that this categorization process is reflected in the face- and body-sensitive N170 component of the ERP wave. Such a perceptual ‘highway’ for processing of sexual cues is highly beneficial for triggering sexual behavior, and subsequently ensuring mating and reproduction. Furthermore, we argue that affective arousal can provide a significant contributory factor in generating the N170 response, providing further support for the models of rapid modulation of visual responses by emotional information [68].

Acknowledgments We thank Pekka Santtila for providing stimulus materials, Ilkka Kirjavainen for his help with data acquisition, and our volunteers for making this study possible.

Author Contributions Conceived and designed the experiments: JKH LN. Performed the experiments: JKH LN. Analyzed the data: JKH LN. Contributed reagents/materials/analysis tools: JKH LN. Wrote the paper: JKH LN.