The main finding of this study is a clear divergence of neuroelectric response to erotic pictures from other picture categories, regardless of their emotional valence or arousal. The present findings suggest that the human brain is able to discriminate rapidly between specific contents of complex visual scenes and that neural representation of the scene meaning can be achieved very early in visual processing. Importantly, this discrimination occurred spontaneously, during free viewing, and in the absence of external cues or explicit response demands (the subjects were not required to make any judgments or responses). The results provide the first evidence for rapid and automatic discriminations of distinct content categories of complex visual scenes in the absence of external cues.
Our results differ from previous studies using complex picture stimuli in several important respects. First, and most important, different neuroelectric responses in our study were associated with a distinct content category (i.e. “eroticism”), rather than with the more general dimensions of emotional valence and arousal that have served as the theoretical framework for previous ERP studies of affective pictures. Second, relatively early content-specific ERP effects were observed over frontal regions, whereas previous studies involving emotional pictures focused mainly on posterior regions of the scalp. Third, this fronto-central activity occurred significantly earlier than the late positive potentials described in previous studies. Finally, in this study, the discrimination of content categories occurred during passive viewing of the pictures and was spontaneous and internally driven, since the subjects were not asked to make evaluative judgments and/or motor responses to specific categories of pictures.
Importantly, the pictures were discriminated by the meaning (biological and/or social) of the depicted situation, rather than merely by the presence or absence of a certain class of objects. It is reasonable to assume that discrimination between erotic and non-erotic scenes should involve even more complex processing compared to other possible types of categorization, such as presence the of humans or faces in the picture, etc. It remains to be seen whether erotic content is unique in eliciting such a distinct neural response. A somewhat puzzling finding of the present study is that emotionally negative pictures (or their specific subcategories) were not discriminated from neutral and positive non-erotic pictures, despite their apparent biological relevance. It is reasonable to speculate that the rapid processing of negative pictures involves, at least partially, different neural circuits. In particular, the fast subcortical visual pathway involving the amygdala (Pessoa, 2005
) may be more involved in the processing of threat-related scenes and the activation of this circuit may not be readily detected by the scalp-recorded ERP.
The present findings challenge the widespread view that ERP responses to affective pictures reflect the overall level of emotional arousal. In our study, early ERP components elicited by erotic scenes were clearly dissociated from other positive emotional pictures, suggesting that early frontal positivity is related to specific content, rather than to positive emotional valence of the picture. The normative female valence ratings for erotic pictures (Lang et al., 1999
) were actually lower
than for positive non-erotic pictures (6.1 and 7.6, respectively). These differences cannot be explained by emotional arousal either, since erotic and positive non-erotic pictures did not differ with respect to their normative arousal ratings (average of 5.9 in both categories). Moreover, negative pictures had the highest arousal ratings (7.0) but did not differ significantly from neutral pictures (3.2) with respect to the anterior ERP response in the 200−600 ms window.
A direct comparison of our results concerning the early anterior effects with previous ERP studies is complicated by the fact that most of these studies used the traditional picture categorization by emotional valence. Very few ERP studies that distinguished specific content categories, including erotica focused on responses in posterior brain regions (Schupp et al., 2004a
, Schupp et al., 2004b
). Nevertheless, the present findings are in line with the observation made in some previous studies that pleasant pictures elicited a larger electrocortical positivity at frontal sites relative to negative and neutral pictures (Diedrich et al., 1997
, Palomba et al., 1997
, Cuthbert et al., 2000
, Amrhein et al., 2004
). Cuthbert et al. (2000)
interpreted this finding in terms of arousal, since in their sample (predominantly male) positive pictures also elicited greater skin conductance responses (SCR). However, other authors (Amrhein et al., 2004
) did not find such difference in SCR and tentatively interpreted this finding as a valence effect, but noted that alternative picture characteristics other than valence need to be ruled out. The present study using alternative categorizations of pictures (by contents vs. by valence) helps to resolve this important issue. When picture were categorized by valence ratings, i.e. erotic and non-erotic positive pictures were in the same category, our results were in good agreement with the above studies (, Supplementary Fig. 2
). Although the most prominent ERP effect was an LPP enhancement for both positive and negative pictures relative to neutral ones, a small but significant (p<0.001) early positive shift was observed for positive pictures relative to negative and neutral pictures. However, further categorization of pictures by content () clearly shows that the early anterior effect is produced entirely by erotic pictures, whereas no significant differences were observed among positive non-erotic, neutral, and negative pictures.
The results obtained for the late positive potential (time window 900−1800 ms) replicate previous findings (Cuthbert et al., 2000
): mean amplitudes for positively and negatively valenced pictures were significantly larger than for the neutral pictures. Consistent with Schupp et al. (2004a)
, this effect was most pronounced for erotic pictures.
Overall, our findings suggest that ERP response to complex visual scenes reflect at least two major stages of processing. The first stage includes a rapid and phasic response that is content-specific and reflects the discrimination of the contextual meaning of the scene. This stage is followed by a more tonic response that is likely to reflect attention allocation during sustained viewing of motivationally relevant information (Cuthbert et al., 2000
, Schupp et al., 2000
, Amrhein et al., 2004
). The existence of functionally distinct modes of processing within relatively narrow time windows underscores the utility of electrophysiology methods for the detection of transient, short-lived, but fundamentally important stages of neural processing. Our findings indicate a rapid, selective, and content-specific processing of erotic materials which can be dissociated from other picture categories regardless of their emotional valence and arousal. One possible interpretation of this finding could be the existence of specialized neural networks for preferential processing of specific categories of stimuli with high adaptive and evolutionary significance.
Previous studies suggest a top-down regulation of sensory processing based on early categorization of visual scenes (e.g. Foxe and Simpson, 2002
). One can speculate that erotic content engages a highly selective neuronal network starting at about 180 ms after picture onset. The activity of this network modulates subsequent processing of the picture, which is reflected in a distinct positive shift of the scalp potential. This modulation may involve suppression of the processing of other, competitive visual information in order to ensure facilitated processing of information of high biological significance.
The specific neural substrates underlying this rapid spontaneous discrimination of picture content remain to be determined. The divergence of neuroelectric responses to different picture categories starts in anterior regions of the scalp, suggesting an involvement of the prefrontal cortex in the discrimination of specific contents. The prefrontal cortex receives projections from the inferior temporal cortex responsible for higher-level object processing. It has been shown recently that the prefrontal cortex of monkeys contains neurons that respond differently to specific categories of complex visual images regardless of their physical similarity (Freedman et al., 2003
). These data, as well as data from neuroimaging studies of visual scene categorization (Fize et al., 2000
) and processing of erotic content (Karama et al., 2002
, Stark et al., 2005
) suggest that a selective, content-specific processing of erotic material is likely to engage areas in the prefrontal and anterior cingulate cortex. Moreover, one of these fMRI studies indicated that early differential ERP responses related to the categorization of natural images can be generated by activity in the fusiform gyrus and cingulate cortex (Fize et al., 2000
). Our finding that the earliest discrimination between picture categories occurs in the frontal midline region is in good agreement with the above studies implicating prefrontal and anterior cingulate cortices in the processing of complex object categories and erotic contents in particular. However, the limited spatial resolution of the EEG and the modest number of electrodes used in this study precludes further speculations about the cortical localization of the effects reported here.
Studies using affective pictures noted stronger subjective and autonomic response to positive, particularly erotic, stimuli in men than women, whereas women were more reactive to threatening stimuli than men (Bradley et al., 2001b
). A recent neuroimaging study (Sabatinelli et al., 2004
) showed that erotic pictures elicited a greater activity in extrastriate visual cortex in men compared with women, suggesting a male visual bias for erotic stimuli. Our findings, however, indicate a strong selectivity of ERP responses to erotic contents in women, suggesting that “erotic bias” can exist in both genders, although the extent to which it is expressed may depend on research methods, in particular their temporal and spatial resolution. Potential gender differences of the effects reported here should be a matter of future studies. Our preliminary data from another study including 18 males and using the same experimental paradigm but slightly different recording parameters indicate a similar frontal positivity effect, the size of which is comparable to the effect reported here for female subjects.
Several alternative explanations of our findings, other than content-specific processing of erotic material, should be considered. First, there is a possibility that the differing ERP responses described here can be caused by systematic differences between erotic and non-erotic pictures with respect to picture characteristics unrelated to their erotic vs. non-erotic content. Pictures may differ with respect to low-level, physical properties such as shape, orientation, brightness, and overall complexity. In our experiments, pictures were equated with respect to the color resolution and the color palette. Careful inspection of images in different content categories does not suggest any systematic differences between erotic and non-erotic pictures with respect to physical properties, overall complexity, or composition. It should be noted that due to multidimensionality of physical and statistical properties of complex natural pictures it is practically impossible to match pictures with respect to such properties.
Apart from low-level features, ERP differences can be attributed to higher-level features such as the presence of humans in the scene or, more specifically, the presence of nude or partially nude humans in the picture. However, post-hoc analyses using alternative picture groupings did not support this hypothesis. There was no significant difference between ERP responses to non-erotic pictures containing images of largely unclothed humans and non-human images. However, this alternative hypothesis needs to be tested more systematically in future studies by comparing responses elicited by erotic scenes with responses produced by images of nude bodies of the same and opposite sex, including both erotically attractive and non-attractive images.
Another possibility is that differing responses to a distinct stimulus category can be related to selective attention directed to this category. Recent studies suggest that the processing of emotionally significant stimuli is not completely automatic and may be subject to top-down attentional modulation (reviewed in Pessoa, 2005
). However, this explanation also seems unlikely, since both positive and negative emotional pictures can draw attentional resources, which is believed to be reflected in a larger late positive potential elicited by such stimuli (Cuthbert et al., 2000
). It is also important that processing of images in this study was spontaneous and unrestricted. Participants viewed the pictures freely and were not instructed to categorize, name, match, or evaluate the pictures, or to make any responses. Thus, no categorical templates were imposed, in contrast to studies using object categorization tasks, where the processing of the target objects could be primed by an instruction-induced internal template.
It should be noted that while the group data presented here reflect overall trends, large individual differences in responses were observed. The nature and significance of these individual differences should be a matter of future analyses. The present findings may also have practical implications, since ERP modulation by erotic content may provide an objective measure of the responsiveness of sex-related motivational systems, dysfunction of which is present in some neuropsychiatric disorders, such as major depression and substance use disorders. Studies conducted using patient groups could determine whether ERPs elicited by erotic and other contents can assist in the diagnosis and treatment evaluation of such disorders.
Several limitations of the present study need to be acknowledged. First, analyses reported here are based solely on a female sample. Our preliminary results from a sample of males tested in another study using the same experimental paradigm are in good agreement with the results reported here, however, direct quantitative comparison of the samples is problematic due to some differences in EEG recording parameters. Therefore, further research is needed to examine possible gender differences in the reported effects. Second, it is not entirely clear whether the observed effect is specific to the erotic context of the depicted social interaction, or it is caused by erotically appealing nude or partially nude bodies of the opposite or same gender. Although our post-hoc analyses suggest that partial nudity alone does not produce the same kind of effect as observed for erotic pictures, more systematic comparisons of pictures are needed in order to elucidate the relative contribution of specific factors, such as nudity, gender, physical attractiveness, and dyadic interaction. For example, future studies should compare responses produced by the same vs. opposite gender nudes, attractive vs. non-attractive nudes, single nudes vs. erotic pairs, etc. Next, the subjects were not required to evaluate each picture on valence and arousal scales in order to ensure that picture viewing is not biased by externally imposed categorical templates. Therefore, normative ratings were used for categorization of pictures based on valence and arousal. Given the large sample size used in this study, it is unlikely that average ratings in our sample would deviate from normative ratings in any significant way, especially since the origin, gender, and age range of our sample was very similar to the sample on which the normative ratings were obtained (Lang et al., 1999
). Furthermore, significant correlations between normative arousal (but not valence) ratings and the late positive potential indicated that the normative ratings applied very well to this sample. Finally, the relatively small number of EEG electrodes used in this study precludes an accurate localization of the sources of electrical activity.
In conclusion, our findings suggest that, in the absence of explicit instruction, the brain is capable of a rapid spontaneous discrimination of complex visual scenes on the basis of their specific biological and/or social meaning.