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Direct intracranial recording of body-selective responses in human extrastriate visual cortex Gilles Pourtois a,b,∗ , Marius V. Peelen a,b , Laurent Spinelli c,d , Margitta Seeck c,d , Patrik Vuilleumier a,b a

Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland b Laboratory for Behavioral Neurology & Imaging of Cognition, Department of Neuroscience & Clinic of Neurology, University of Geneva, Geneva, Switzerland c Pre-surgical Epilepsy Evaluation Unit, Clinic of Neurology, University Hospital, Geneva, Switzerland d Functional Brain Mapping Laboratory, Department of Neuroscience, University of Geneva, Geneva, Switzerland Received 12 February 2007; received in revised form 3 April 2007; accepted 3 April 2007

Abstract We recorded intracranial local field potentials (iLFPs) in right extrastriate visual cortex of a patient prior to surgery for epilepsy. Visual evoked potentials revealed a highly selective response to images of bodies, relative to faces, mammals, and tools, which was restricted to a focal region in the lateral occipitotemporal cortex that corresponds to the location of the extrastriate body area (EBA). Body-selective activity started around 190 ms and peaked 260 ms post-stimulus onset. These findings provide the first direct electrophysiological evidence for an early visual processing stage in human lateral occipitotemporal cortex that is specialized for processing human body shapes. © 2007 Elsevier Ltd. All rights reserved. Keywords: Body perception; Intracranial recording; Epilepsy

1. Introduction Recent evidence from neuroscience research suggests that specific regions within the primate visual cortex are organized according to specific object-category preferences, including not only regions selectively responsive to faces (Gross, 1992; Halgren et al., 1999; Kanwisher, McDermott, & Chun, 1997; Puce, Allison, Gore, & McCarthy, 1995; Tsao, Freiwald, Knutsen, Mandeville, & Tootell, 2003), but also other regions responsive to bodies and body parts (Desimone, Albright, Gross, & Bruce, 1984; Downing, Jiang, Shuman, & Kanwisher, 2001; Peelen & Downing, 2005; Pinsk, DeSimone, Moore, Gross, & Kastner, 2005; Wachsmuth, Oram, & Perrett, 1994). In particular, human fMRI studies have revealed that a relatively circumscribed area within the lateral occipitotemporal cortex shows selective activation to pictures of human bodies, relative ∗ Corresponding author at: Swiss Center for Affective Sciences, 7 rue des Battoirs, CH-1205 Geneva, Switzerland. Tel.: +41 22 37 99 814; fax: +41 22 37 99 844. E-mail address: [email protected] (G. Pourtois).

to other object categories, including faces or animals (Downing et al., 2001). This body-selective area is typically located at the posterior end of the inferior temporal sulcus, and has been termed the extrastriate body area (EBA; Downing et al., 2001). The body selectivity of EBA has been tested using a wide variety of control visual stimuli, such as faces, mammals, tools, or landscapes (Downing, Chan, Peelen, Dodds, & Kanwisher, 2006a; Downing, Peelen, Wiggett, & Tew, 2006b), and appears relatively independent of the low-level visual features of body stimuli. Indeed, the EBA also responds selectively to schematic representations of bodies, such as stick figures or silhouettes, versus visually similar controls (Downing et al., 2001). In monkeys, hand-selective cells have also been observed in temporal visual cortex (Desimone et al., 1984; Wachsmuth et al., 1994), and more recently, monkey fMRI studies have shown a bodyselective region on the ventral bank of the STS, neighbouring a face-selective area (Pinsk et al., 2005). However, fMRI is an indirect measure of neuronal activity, with limited temporal resolution. Therefore, the time-course of body-selective responses in this region of human visual cortex is still entirely unknown.

0028-3932/$ – see front matter © 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2007.04.005

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Only very few electrophysiological studies have been conducted in humans to investigate the visual processing of body shapes. A pioneering intracranial recording study (McCarthy, Puce, Belger, & Allison, 1999) reported category-selective responses for various stimuli, such as faces, hands, or flowers that arose at several electrode sites in posterior brain regions, typically 200–250 ms after stimulus onset, and located in various cortical areas, including ventral temporal cortex, left superior temporal sulcus, and left inferior parietal cortex. However, no data was reported for the lateral occipitotemporal regions that were identified as EBA by subsequent fMRI studies. More recent work measuring event-related potentials on the scalp has also reported body-selective responses, characterised by a negative activity at 190 ms after stimulus onset and a distinct topographical distribution of electrical activity at the scalp surface (Thierry et al., 2006). However, it remains unclear whether these bodyselective responses measured by EEG over the scalp may relate to any specific cortical region, and more particularly to EBA as observed in fMRI studies. Anatomically, the EBA overlaps with motion-selective MT+ and object-selective LO, although it can be partly dissociated from these two regions (Downing, Wiggett, & Peelen, 2007). Nevertheless, it is unknown whether body-selective responses in EBA relate to an early perceptual stage of visual analysis (as expected if it corresponds to body-shape processing), or to later stages that might potentially result from feedback to motion-related processes, perhaps associated with imagery of body movements (de Gelder, 2006). Importantly, results from recent TMS experiments indicate that body recognition may be impaired after stimulation of the EBA (Urgesi, Berlucchi, & Aglioti, 2004), suggesting that the EBA is necessary for successful recognition of bodies. In the present study, we had the unique opportunity to record iLFPs from the lateral occipitotemporal in a human patient, prior to surgery for pharmacoresistant epilepsy. Exceptionally, this patient had an electrode grid placed over extrastriate cortex, which included the location of the EBA, and covered an extensive portion of occipital lobe that is rarely investigated by depth-electrodes in human patients (Clarke, Halgren, Scarabin, & Chauvel, 1995; Convers et al., 1990; Seeck et al., 2001). This allowed us to establish, for the first time, the electrophysiological signature of body-selective responses in this region. 2. Methods 2.1. Experimental procedure We recorded electrophysiological responses in a 27-year-old right-handed male patient, who suffered from epilepsy since the age of 17 years. His seizures were characterized by a brief loss of consciousness, with automatic gestures and wandering eye movements, but no convulsive movements. Detailed neuropsychological assessment showed no cognitive impairment, and the patient worked part-time as an accountant. Before electrode implantation, he was treated by regular anti-epileptic drugs (leviracetam and carbamazepin); but at the time of our testing he was free of any medication, according to a standard weaning protocol in the pre-surgical evaluation unit. He was tested during a pre-surgical evaluation phase in a clinical setting, while undergoing intracranial EEG with subdural electrodes to identify the epilepsy focus. The electrode grid was placed over the lateral surface of the right hemisphere, covering the posterior temporal and ante-

rior occipital cortex (Fig. 1A). The patient was shown various black and white static images of faces, human bodies, mammals, and tools (see Downing et al., 2006a,b), presented sequentially for 500 ms each, in a pseudo-random order (40 different images per category × 4 visual categories). The patient was asked to categorize each stimulus using a 4-button response box (four-alternative forced choice). Stimuli were shown on a computer screen at a viewing distance of 1 m (all with the same homogenous grey-level background and the same size: 400 pixels width × 400 pixels height). Inter-trial interval was 1250 ms. The patient correctly discriminated the four object categories on 97% of trials (mean RTs: 656 ms for faces, 705 ms for bodies, 683 ms for mammals, and 645 ms for tools).

2.2. Data recording Intracranial LFPs were continuously recorded (Ceegraph XL, Biologic System Corps.) with a sampling rate of 512 Hz (bandpass 0.1–200 Hz) using 24 subdural stainless electrodes (AD-Tech, electrode diameter: 6 mm, interelectrode spacing: 10 mm) distributed evenly over the cortical surface (6 × 4 electrodes grid array, see Fig. 1A). The reference electrode was located at position Cz and the ground at position FCZ in the 10–20 international EEG system. Intracranial visual evoked potentials (VEPs) were obtained by averaging LFPs time-locked to stimulus onset, for each object category separately. Individual epochs were low-pass filtered using a 30 Hz cutoff. Electrode positions were determined by a brain CT-scan performed after implantation, and coregistered using SPM5 (http://www.fil.ion.ucl.ac.uk/spm/software/spm5/) to the patient’s brain anatomy as obtained with MRI, which in turn was Talairach normalized in order to define Talairach coordinates of each of the recorded electrodes.

2.3. Data analysis Single-trial EEG epochs were analyzed offline, after removing all epochs where co-occurring epileptic spikes might have spread and contaminated the recorded site (∼25%, using stringent visual inspection). The amplitude variance computed for each time-point across these trials was then used as dependent variable for statistical comparisons. To determine whether body-selective responses were stable over time and across trials, we first computed an amplitude × time image for all consecutive presentations of body pictures (Delorme & Makeig, 2004). Body selectivity was next verified by performing a series of nonparametric statistical analyses based on stringent randomization tests (Manly, 1991). The significant alpha cutoff was set to p < 0.001, with an additional criterion of temporal stability for 10 consecutive time-points (>20 ms at 512 Hz sampling rate). Randomization provides a robust non-parametric method to test for differences in any variable (here amplitude at each time-point) without any assumption regarding data distribution, by comparing the observed dataset with random shuffling of the same values over many iterations. The method runs by repeating the shuffling many times (minimum of 5000 with the randomization tests used here) so as to be able to estimate the probability (here p < 0.001) that the data might be observed by chance. First, we compared the amplitude variance at each individual time-point (from −1000 ms to +1500 ms post-stimulus onset at 512 Hz) to the mean baseline activity (computed from −1000 ms to stimulus onset), in order to identify the exact onset of body-selective responses relative to baseline. Second, we performed direct pairwise comparisons between categories (body versus face; body versus mammal; body versus tool) using similar randomization tests for each individual time-point (from −1000 to +1500 ms post-onset). These analyses were performed using the Cartool software by Denis Brunet (http://brainmapping.unige.ch/Cartool.php).

3. Results Fig. 1B shows the VEPs for each of the four conditions across the 24 electrodes covering the lateral occipitotemporal cortex (Fig. 1A). One electrode, contact #15, showed a very selective response to images of human bodies compared to images of faces, mammals, and tools. The Talairach coordinates of this electrode (x = +39, y = −77, z = −2) fell within the range of

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Fig. 1. (A) Right back view of the brain anatomy of the patient (MRI T1-weighted reconstructed brain volume), showing the exact location of the grid with 6 × 4 subdural electrodes covering the lateral and inferior part of right occipital cortex. (B) For each recording site, VEPs are shown for faces (black trace), bodies (red trace), tools (blue trace) and animals (green trace). Time is plotted along the x axis, from −200 to +500 ms around stimulus onset. Amplitude is plotted along the y axis, from +150 ␮V (down) to −150 ␮V (up). (C) VEPs recorded for each visual category (faces, black trace; bodies, red trace; tools, blue trace and animals, green trace) are plotted for the critical electrode (#15), showing clear stimulus-locked responses with an early (onset: 190 ms post-stimulus; peak: 260 ms), ample (−135 ␮V amplitude), and sustained negative activity for bodies relative to faces, tools, and mammals. Time is plotted along the x axis, from −500 to +1500 ms around stimulus onset. Amplitude is plotted along the y axis, from +100 ␮V (down) to −160 ␮V (up). (D) ERP image (2D image transformations of individual epoched data, see Delorme & Makeig, 2004) computed for all single trials (electrode #15) in the condition with body pictures. Trial order is represented along the y axis, from trial #1 (down) to trial #40 (up). Time is plotted along the x axis from −1000 to +1500 ms around the stimulus onset. The amplitude of each single-trial response is plotted from −150 ␮V (blue color) to +150 ␮V (red color). This trial-by-trial breakdown of the data demonstrated that a reliable negative deflection occurred ∼200 to ∼800 ms post-onset for all successive (though physically different) body pictures. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

previously reported coordinates for EBA (x = +48 [S.D. = 5], y = −70 [5], z = 1 [6]; see Peelen, Wiggett, & Downing, 2006). We statistically verified the body selectivity of this electrode using two different non-parametric randomization tests (see Section 2). The first analysis revealed that electric neural activity generated by body images began to differ reliably from baseline activity 190 ms post-stimulus onset, and then remained significantly different (p < 0.001) from baseline for the next 450 ms. This highly significant activation consisted of an initial negative peak (maximum amplitude: −135 ␮V, maximum latency: 260 ms), followed by a slower and sustained deflection (Fig. 1C). By contrast, other categories evoked less selective visual responses and differed more weakly from baseline, from 200 ms onwards. Secondly, pairwise non-parametric statistical comparisons of the different visual categories disclosed a highly significant (p < 0.001) and stable difference between bodies versus faces (starting 190 ms post-onset, temporal duration 380 ms, mean amplitude −86.3 versus −8.9 ␮V, respectively); as well

as between bodies versus tools (starting 218 ms post-onset, stability 86 ms, amplitude −42.8 ␮V); and between bodies versus mammals (starting 256 ms post-onset, duration 48 ms, amplitude −46.4 ␮V). In all cases, these differences reflected a larger negative deflection for bodies than other categories. The comparison between tools and mammals revealed no significant difference during the whole epoch (from −1000 to +1500 ms post-onset), indicating that these two categories produced similar neural responses in this area. Images of mammals and tools both elicited a stronger response than faces (both p’s < 0.01), which produced the weakest visual response among all categories (see Fig. 1C). Similar statistical analyses on the other 23 electrodes did not show significant selectivity for any of the four object categories, and thus confirmed that body-selective responses were highly specific to electrode #15. As shown by the ERP image in Fig. 1D (Delorme & Makeig, 2004), body-selective responses were clearly visible on a trial-by-trial basis, very reproducible over time, and precisely time-locked to the stimulus presentation.

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4. Discussion

Acknowledgements

The present results shed new light on the time course and spatial specificity of body-selective responses in human lateral occipitotemporal cortex. We show that body-selective responses start at 190 ms and peak at 260 ms post-stimulus onset in a focal region of extrastriate visual cortex, comprising one subdural electrode only. The location of this electrode corresponds remarkably well to that of EBA as reported in previous fMRI studies (Peelen et al., 2006). The time course of neural responses recorded in this electrode also accord with the recently reported body-selective N190 (Thierry et al., 2006), which suggests that EBA might constitute the source of this peak and of the corresponding topographic map at the level of the scalp, with minimal contribution of other cortical sites observed in the study of McCarthy et al. (1999). The early time course of body selectivity reported here is consistent with a major role for EBA in the initial perceptual analysis of body shapes, rather than a more delayed process arising at later stages (e.g. through top-down effects related to imaginary gestures and movement). In keeping with this, TMS results showed that disrupting activation in this area at 150–250 ms post-stimulus onset may impair performance on a match-to-sample task with images of body parts, but not with images of face or motorcycle parts (Urgesi et al., 2004). Although this TMS study did not test other time windows, our results would indeed predict the strongest effects of TMS at a latency between 200 and 300 ms. Another recent TMS study of EBA, using a similar design (except for a stimulation latency of 150–350 ms), showed a stronger impairment for tasks involving discrimination of body form versus body actions (Urgesi, Candidi, Ionta, & Aglioti, 2007). Previous fMRI studies have similarly suggested that the EBA maintains a static representation of human body shape (Downing et al., 2006a,b), and that it may constitute a critical early stage in the perception of other people (Chan, Peelen, & Downing, 2004). The observation that the electrode with strong bodyselectivity is also responding somewhat at the same latency (but to a much lesser extent) to pictures of tools may indicate some relation to cortical processes specialized for extracting motor or action-related information (Astafiev, Stanley, Shulman, & Corbetta, 2004). Likewise, pictures of mammals, which include non-human bodies and body parts, also elicited a stronger response than faces, a pattern similar to the results for EBA in fMRI studies (Downing et al., 2006a,b). It remains unknown whether this pattern of body selectivity that emerged against other categories at different time-points, following a nonselective initial response, might reflect any functional property of the underlying neuronal computations. Taken together, these studies point to a relatively early implication of EBA in processing stages associated with the perception of human bodies. Future studies should clarify how this area may interact with other cortical regions involved in perceiving other people, such as the fusiform gyrus, superior temporal sulcus, and action-related frontal and parietal regions.

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