Elsevier

Cortex

Volume 134, January 2021, Pages 239-252
Cortex

Research Report
Like the back of my hand: Visual ERPs reveal a specific change detection mechanism for the bodily self

https://doi.org/10.1016/j.cortex.2020.10.014Get rights and content

Abstract

The ability to identify our own body is considered a pivotal marker of self-awareness. Previous research demonstrated that subjects are more efficient in the recognition of images representing self rather than others' body effectors (self-advantage). Here, we verified whether, at an electrophysiological level, bodily-self recognition modulates change detection responses. In a first EEG experiment (discovery sample), event-related potentials (ERPs) were elicited by a pair of sequentially presented visual stimuli (vS1; vS2), representing either the self-hand or other people's hands. In a second EEG experiment (replicating sample), together with the previously described visual stimuli, also a familiar hand was presented. Participants were asked to decide whether vS2 was identical or different from vS1. Accuracy and response times were collected. In both experiments, results confirmed the presence of the self-advantage: participants responded faster and more accurately when the self-hand was presented. ERP results paralleled behavioral findings. Anytime the self-hand was presented, we observed significant change detection responses, with a larger N270 component for vS2 different rather than identical to vS1. Conversely, when the self-hand was not included, and even in response to the familiar hand in Experiment 2, we did not find any significant modulation of the change detection responses. Overall our findings, showing behavioral self-advantage and the selective modulation of N270 for the self-hand, support the existence of a specific mechanism devoted to bodily-self recognition, likely relying on the multimodal (visual and sensorimotor) dimension of the bodily-self representation. We propose that such a multimodal self-representation may activate the salience network, boosting change detection effects specifically for the self-hand.

Introduction

The ability to recognize the own body visually (for example from a picture or when it is reflected in the mirror) has traditionally been considered as a pivotal marker of self-awareness (for a recent review see e.g., Apps & Tsakiris, 2014). However, while we usually distinguish other people's body by vision only, for bodily-self recognition we can rely on information coming from different sensory modalities (Tsakiris, 2010). To identify own body effectors, we usually resort to a wide network of sensorimotor (e.g., proprioceptive, somatosensory, and motor) inputs, rather than to visual features per se (Ehrsson, Holmes, & Passingham, 2005; Frassinetti, Ferri, Maini, Benassi, & Gallese, 2011). Nonetheless, in a series of previous studies employing visual-matching tasks, Frassinetti and colleagues demonstrated that subjects are faster and more accurate in discriminating grey-scale pictures representing bodily-self effectors as compared to others' body effectors (the so-called self-advantage) (Frassinetti et al., 2008, 2009, 2011). The presence of such facilitation in participants' performance has been associated with the recourse to a sensorimotor network recruited when subjects had to recognize the bodily-self in “implicit” tasks (see e.g., Frassinetti et al., 2009; Conson, Volpicella, De Bellis, Orefice, & Trojano, 2017; in other words, the self-recognition is task-irrelevant, i.e., not explicitly required in task instructions). More specifically, the self-advantage was associated with the activation of a visual-sensorimotor network including, besides occipital areas, bilateral premotor cortex, and right temporal cortex encompassing the extrastriate body area (Ferri, Frassinetti, Ardizzi, Costantini, & Gallese, 2012). However, even though the study by Ferri and colleagues revealed a direct involvement of the somatosensory cortices in self-hand recognition, since a motor task (i.e., hand-rotation) was performed, it cannot be excluded that the (motor) nature of the task might have contributed to the observed sensorimotor activation.

The idea that bodily-self recognition implies the interaction between visual and sensorimotor areas has been confirmed also by different lines of research that does not employ motor tasks, such as those studies investigating the neural correlates of a famous illusion of body ownership (i.e., the rubber hand illusion; see e.g., Botvinick & Cohen, 1998; Bucchioni et al., 2016; Burin et al., 2017; Della Gatta et al., 2016; Fossataro, Bruno, Giurgola, Bolognini, & Garbarini, 2018). During this illusion, participants, while watching a human-like rubber hand being touched synchronously with their own hand hidden from view, experience the feeling that the fake hand has become part of their own body. It has been demonstrated that, during this procedure, the functional connectivity between visual areas (e.g., lateral occipitotemporal cortex and extrastriate body area; EBA) and ventral premotor cortex is specifically modulated during the embodiment (i.e., when the fake hand is attributed to themselves) (Limanowski & Blankenburg, 2015; Zeller, Friston, & Classen, 2016), consistently with the fact that the illusion reduces the perceived objective (visual) dissimilarities between the own and the rubber hand (Longo, Schuur, Kammers, Tsakiris, & Haggard, 2009). Moreover, lesion studies of brain-damaged patients exhibiting an impairment of self-other hands discrimination support the involvement of a visual-sensorimotor network in self-recognition (Garbarini, Fossataro, Pia, & Berti, 2020). Indeed, the core lesion underpinning this deficit has been identified in the subcortical white matter connecting temporal areas, involved in the visual recognition of the body (i.e., the extrastriate body area, EBA), with anterior multisensory areas, such as the premotor cortex (Pia et al., 2020).

Furthermore, the recruitment of multimodal networks (including sensorimotor areas) in self-recognition is not only observed for limb discrimination, but it has been described for faces as well, without the involvement of a motor task (Cardini et al., 2011; Morita et al., 2018; Sugiura, 2015). For example, Cardini and colleagues found that ventral premotor cortex activity differed when viewing self-face as compared to another's face, thus revealing a crucial role of sensorimotor areas in self-other face discrimination. Accordingly, the processing of the self-face has been associated with a specific sensorimotor pattern of activations, involving sensory (i.e., visual, somatosensory, and interoceptive areas) and motor association cortices (i.e., premotor cortex and supplementary motor area – see Sugiura et al., 2015 for a review). Overall these findings suggest the presence of different mechanisms for self-versus other people's body recognition (De Bellis, Trojano, Errico, Grossi, & Conson, 2017; Ferri, Frassinetti, Costantini, & Gallese, 2011; Hu et al., 2016; Myers & Sowden, 2008), thus highlighting the specificity of self-recognition.

In the present study, we investigated whether implicit (task-irrelevant), bodily-self recognition has an observable electrophysiological correlate. To this aim, we exploited the repetition suppression phenomenon and we asked whether it could be modulated by implicit, bodily-self recognition. As widely described in the literature, event-related potential (ERP) amplitudes are strongly reduced when the same stimulus is repeated at short and constant time intervals (Iannetti, Hughes, Lee, & Mouraux, 2008; Wang, Mouraux, Liang, & Iannetti, 2010). Amplitude modulations induced by repetition have also been observed for abstract visual stimuli, such as different shapes (Wang, Cui, Wang, Tian, & Zhang, 2004), and body-related pictures, mainly human faces (for a recent review see Schweinberger & Neumann, 2016). Importantly, the detection of a change within the stimulus sequence is able to revert such amplitude reduction due to repetition. In other words, the sudden change of one or more stimulus basic features (e.g., modality, intensity, shape, or color) usually enhances the amplitude of the evoked responses (Valentini, Torta, Mouraux, & Iannetti, 2011; Wang et al., 2004). However, this is not always the case. Through a paradigm exploiting intensity modulations of repeated painful stimuli, it has been shown that intensity increases but not decreases could revert repetition-related amplitude reduction (Ronga, Valentini, Mouraux, & Iannetti, 2013). The authors interpreted their findings suggesting that only salient changes were able to induce change detection-related responses.

Based on the above evidence, changes involving the self-hand should be considered salient by the nervous system. Previous studies highlighted the specificity of self-hand recognition, which seems to rely on a peculiar sensorimotor mechanism. In other words, the difference between the self-versus other people's hand recognition, by resorting to distinct neural mechanisms, may represent a kind rather than a degree property. It seems therefore likely that stimulus changes involving the self-hand may elicit salience effect (i.e., the reversion of repetition suppression), which are similarly described as kind phenomena. Indeed, as demonstrated by previous studies (Ronga et al., 2013; Torta, Liang, Valentini, Mouraux, & Iannetti, 2012), the change detection effects induced by salient stimuli are expressed in an all or nothing fashion (i.e., the reversion of repetition suppression is not gradable but either present or absent). Analogously, since the self-hand could be more salient than the other's hands, we should expect that only the visual presentation of the self-hand may induce change detection-related responses. Conversely, changes between other people's hands, and even between familiar and not familiar hands, may not be salient enough to revert repetition suppression phenomena.

In our EEG paradigms, ERPs were recorded while participants were presented with grey-scale images depicting the right hands. Hand pictures were delivered in pairs (vS1 and vS2), at a constant 1-second interval, and might represent either the participant's self-hand or other people's hands. Experiment 1 was directed to explore whether the presentation of the self-hand boosts the change detection mechanism, reversing the repetition suppression phenomenon. It was divided into two different conditions (scenarios): in the With Self scenario, the self-hand was included within the presented visual stimuli; in the Without Self scenario, the self-hand was never presented (see 2.1.2 for a rationale description). Subjects were asked to judge whether vS2 was identical or different from vS1 (implicit recognition task). ERPs to visual stimuli, as well as accuracy and response times (RTs) were collected. Experiment 2 specifically aimed at replicating the results of Experiment 1 also controlling for any familiarity bias in our behavioral and EEG results. In the design of Experiment 1, the self-hand is the only hand participants had some familiarity with. Therefore, in case we found any specific change detection response for the self-hand, we could not disentangle whether this result was driven by a mechanism specific for the body-self or by a general familiarity effect. To control for this aspect, in Experiment 2 we included a third scenario, namely the With Familiar scenario, where one of the two others' hands was familiar to the participants, through repeated presentation of such a hand in the immediately preceding scenario.

From a behavioral point of view, both in Experiments 1 and 2, we expected to confirm the presence of the self-advantage, i.e., higher accuracy and faster RTs any time when at least one self-hand was included in the pair of visual stimuli. From an electrophysiological point of view, if bodily-self recognition actually represents a unique and salient phenomenon, recruiting dedicated mechanisms and neural networks, then in both experiments we should observe a significant change detection effect (i.e., greater amplitude difference between responses to repeated vs non-repeated stimuli) only for images representing the self-hand. Crucially, in Experiment 2 we should observe a clear difference in the change detection responses between the With Self scenario and the With Familiar scenario, with significant change detection effect for the self-hand. We expect that this effect might specifically be observed on the N270 modulation, a component which has been systematically related to visual change detection (Bennett, Duke, & Fuggetta, 2014; Scannella et al., 2016; Wang et al., 2018; Zhang et al., 2008).

Alternative results, showing a similar change detection effect for self- and other people's hands, would instead challenge the idea of the presence of a specific mechanism for bodily-self recognition.

Section snippets

Participants

Fifteen healthy right-handed subjects participated in the study (5 women) aged 22–26 years (mean ± SD: 24.1 ± 1.2; years of education: 17.9 ± 1.0).

Sample size (N = 15) was a priori determined to match the number of subjects involved in previous research investigating visual mismatch detection effects and exploiting the same EEG analyses employed in the present study (Wang et al., 2003, N = 13; Wang et al., 2004, N = 15; Bennet et al., 2014, N = 16).

All participants gave their written informed

Behavioral results

Behavioral results are presented in Fig. 2. Note that, overall are in line with our predictions, participants showed a more accurate and faster behavioral performance anytime the self-hand was included in the pair, thus indicating the presence of the self-advantage effect also in our sample.

Discussion

The present paper, focused on bodily self-identification, explores whether the recognition of our physical identity has an observable electrophysiological correlate. More specifically, we exploited the amplitude modulation following different versus identical stimulation to verify whether implicit bodily-self recognition is able to modulate change detection responses, in a pair of sequentially presented visual stimuli. Importantly, previous literature investigating body-related change detection

Author contribution

Mattia Galigani: conceptualization, methodology, software, formal analysis, investigation, writing and original draft, visualization.

Irene Ronga: conceptualization, methodology, software, formal analysis, investigation, writing and original draft, visualization.

Carlotta Fossataro: software, formal analysis, writing and review and editing.

Valentina Bruno: software, formal analysis, writing and review and editing.

Nicolò Castellani: investigation, writing and review and editing.

Alice Rossi

Funding

This work was supported by the San Paolo Foundation 2016 grant (CSTO165140) to F.G. and by Bando Talenti della Società Civile 2019 to M.G.

Open practices

The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at http://dx.doi.org/10.17632/rz6gcc29dj.1. The present experiments and analyses were not pre-registered. In our methodological section, we report how we determined our sample size, all data exclusions, all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations, and all measures in

Acknowledgement

The authors are grateful to the volunteers involved in the study. The authors declare no conflict of interest.

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