Haptic perception and body representation in lateral and medial occipito-temporal cortices

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Neuropsychologia 49 (2011) 821–829

Contents lists available at ScienceDirect

Neuropsychologia

journa l homepage: www.e lsev ier .com/ locate /neuropsychologia

aptic perception and body representation in lateral and medialccipito-temporal cortices

arcello Costantinia,b,∗,1, Cosimo Urgesi c,d,∗∗,1, Gaspare Galati e,f, Gian Luca Romanig,b,alvatore M. Aglioti e,f

Laboratory of Neuropsychology and Cognitive Neuroscience, Department of Neuroscience and Imaging, University G. d’Annunzio, Chieti, ItalyInstitute for Advanced Biomedical Technologies – ITAB, Foundation University G. d’Annunzio, Chieti, ItalyDipartimento di Scienze Umane, Università di Udine, Udine, ItalyIstituto di Ricovero e Cura a Carattere Scientifico‘Eugenio Medea’, Polo Friuli Venezia Giulia, San Vito al Tagliamento, Pordenone, ItalyDipartimento di Psicologia, Università di Roma ‘La Sapienza’, Roma, ItalyIstituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, I-00179 Roma, ItalyDepartment of Neuroscience and Imaging, University G. d’Annunzio, Chieti, Italy

r t i c l e i n f o

rticle history:eceived 18 March 2010eceived in revised form 17 January 2011ccepted 18 January 2011vailable online 21 February 2011

eywords:aptic explorationxtrastriate body area (EBA)usiform body area (FBA)MRI

a b s t r a c t

Although vision is the primary sensory modality that humans and other primates use to identify objectsin the environment, we can recognize crucial object features (e.g., shape, size) using the somatic modal-ity. Previous studies have shown that the occipito-temporal areas dedicated to the visual processingof object forms, faces and bodies also show category-selective responses when the preferred stimuliare haptically explored out of view. Visual processing of human bodies engages specific areas in lateral(extrastriate body area, EBA) and medial (fusiform body area, FBA) occipito-temporal cortex. This studyaimed at exploring the relative involvement of EBA and FBA in the haptic exploration of body parts. DuringfMRI scanning, participants were asked to haptically explore either real-size fake body parts or objects.We found a selective activation of right and left EBA, but not of right FBA, while participants hapticallyexplored body parts as compared to real objects. This suggests that EBA may integrate visual body repre-

ultimodal body processingody perception

sentations with somatosensory information regarding body parts and form a multimodal representationof the body. Furthermore, both left and right EBA showed a comparable level of body selectivity duringhaptic perception and visual imagery. However, right but not left EBA was more activated during hapticexploration than visual imagery of body parts, ruling out that the response to haptic body explorationwas entirely due to the use of visual imagery. Overall, the results point to the existence of different mul-timodal body representations in the occipito-temporal cortex which are activated during perception andimagery of human body parts.

. Introduction

Accurate perception of the body of other individuals is uniquely

mportant for our social life. Perceiving another person’s bodyllows us to extract crucial social information related to gender,ge, identity, and attractiveness. Recent neuroimaging evidenceemonstrates the existence of specific brain structures involved

∗ Corresponding author at: Department of Neuroscience and Imaging, Universityf Chieti, Via dei Vestini 33, I-66100 Chieti, Italy. Tel.: +39 0871 3556945;ax: +39 0871 3556930.∗∗ Corresponding author at: Dipartimento di Scienze Umane, Università di Udine,ia Margreth, 3, I-33100 Udine, Italy. Tel.: +39 0432 249889; fax: +39 0432 556545.

E-mail addresses: [email protected] (M. Costantini),[email protected] (C. Urgesi).

1 These authors contributed equally to this work.

028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2011.01.034

© 2011 Elsevier Ltd. All rights reserved.

in the visual processing of the human body (Peelen & Downing,2007). Indeed, viewing non-facial body parts selectively engen-ders bilateral activation of a lateral occipito-temporal region calledextrastriate body area (EBA). EBA is activated by viewing partial orwhole movies, photographs or sketchy drawings of human bodiesand body parts but not faces and objects (Peelen & Downing, 2007).More recent fMRI studies have demonstrated the existence ofanother body selective area that is anatomically distinct from EBA.This area, located in the fusiform gyrus and known as fusiform bodyarea (FBA), responds selectively to whole bodies and body parts andis adjacent to and partly overlaps with the fusiform face area (FFA)

(Peelen & Downing, 2005; Schwarzlose, Baker, & Kanwisher, 2005),which is selectively activated by visual presentation of humanfaces (Gauthier et al., 2000; Haxby, Hoffman, & Gobbini, 2000;Kanwisher, McDermott, & Chun, 1997). The research on the pos-sible difference between the body representations housed in the

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22 M. Costantini et al. / Neuro

ateral (EBA) and medial (FBA) occipito-temporal cortex is mea-er. However, a few studies (Hodzic, Kaas, Muckli, Stirn, & Singer,009; Taylor, Wiggett, & Downing, 2007; Urgesi, Calvo-Merino,aggard, & Aglioti, 2007) have suggested that while EBA may beore involved in the detail-based processing of body parts, FBAay be more involved in the configural processing of larger assem-

lies of parts and whole bodies.Although vision is the primary sensory modality that humans

nd other primates use to identify objects and other people in thenvironment, we can also use our sense of touch to perceive thehape, size, texture and other characteristics of objects (Klatzky,ederman, & Metzger, 1985), faces (Kilgour & Lederman, 2002)nd non-facial body parts (Eidelman, Hovars, & Kaitz, 1994; Kaitz,992; Kaitz, Lapidot, Bronner, & Eidelman, 1992; Kaitz, Meirov,andman, & Eidelman, 1993; Kaitz, Shiri, Danziger, Hershko, &idelman, 1994). Importantly, it has been documented a conver-ence of visual and tactile information into occipito-temporal areas,ointing to the existence of a multimodal representation of object,ace, and body forms in the extrastriate visual cortex. In partic-lar, haptic exploration of objects as compared to exploration ofextures engenders activation in the lateral occipital complex areaLOC) (Amedi, Malach, Hendler, Peled, & Zohary, 2001; Amedi,acobson, Hendler, Malach, & Zohary, 2002; James et al., 2002), anxtrastriate occipito-temporal area that was originally describeds responding more to visual presentation of object forms thanextures (Grill-Spector, Kourtzi, & Kanwisher, 2001; Malach et al.,995). Furthermore, the pattern of activation of the extrastriate cor-ex during haptic exploration reflects, in both sighted (blindfolded)nd congenitally blind individuals, the same category-dependentattern observed for visual processing (Pietrini et al., 2004). Insimilar vein, haptic exploration of faces engenders activation

f the fusiform cortex (James, Servos, Kilgour, Huh, & Lederman,006; Kilgour, Kitada, Servos, James, & Lederman, 2005; Kitada,ohnsrude, Kochiyama, & Lederman, 2009), while haptic explo-ation of non-facial body parts activates EBA (Kitada et al., 2009).hese data suggest that FFA and EBA may mediate multimodalecognition of faces and bodies, respectively. On the other hand, theesponse of the FBA to the haptic presentation of body parts has noteen so far investigated and it is unclear whether the haptic rep-esentations of faces and bodies partially overlap in the fusiformortex as their visual representations do (Peelen & Downing, 2005;chwarzlose et al., 2005). In a previous fMRI study (Kitada et al.,009), the haptic identification of hands and feet engendered areater activation with respect to control objects in the EBA butot in the FFA. Since FFA and FBA partially overlap, this resultould suggest that the fusiform cortex is involved in coding visu-lly, but not haptically perceived bodies. However, face and bodyelective areas in the fusiform cortex are only partially overlap-ing at the individual level and high-resolution fMRI techniquesSchwarzlose et al., 2005) or multi-voxel pattern analyses (Peelen,

iggett, & Downing, 2006) reveal the dissociation between face-nd body-selective activations. Thus, the response pattern of FFAannot inform on the possible activation of FBA to haptic bodyerception. The present study was aimed at comparing the acti-ation of EBA and FBA during haptic exploration. We used fMRIo localize the EBA and FBA activations with a visual perceptionask and measured their response pattern during the haptic explo-ation of body parts and objects. Furthermore, to rule out that EBAnd FBA activation during haptic exploration was simply due toisual imagery of the touched body part (Kilgour & Lederman, 2002;itada et al., 2009; Lederman, Klatzky, Chataway, & Summers, 1990;

hang, Weisser, Stilla, Prather, & Sathian, 2004), in separate blockse also asked participants to imagine, visually or haptically, bodyarts and objects.

Based on previous studies of object (Amedi et al., 2001, 2002;ames et al., 2002), face (James et al., 2006; Kilgour, Servos, James,

ologia 49 (2011) 821–829

& Lederman, 2004; Kitada et al., 2009; Pietrini et al., 2004) andbody (Kitada et al., 2009) haptic recognition, we could predict thathaptic body processing activates body-selective areas in the lat-eral (EBA) as well as medial (FBA) occipito-temporal cortex. On theother hand, while EBA seems more involved in the visual process-ing of body part details (Taylor et al., 2007; Urgesi, Calvo-Merino,et al., 2007), FBA may be more involved in the configural processingof body identities (Hodzic et al., 2009; Taylor et al., 2007). As hapticexploration involves a sequential processing of piecemeal infor-mation (Kitada et al., 2009; Lederman & Klatzky, 1990), we couldexpect higher activity in EBA than FBA during haptic processing ofbody parts.

2. Materials and methods

2.1. Participants

Thirteen neurologically normal subjects (19–24 years, 12 females) took part inthis study after giving written informed consent. All were right-handed as defined bythe Italian version of the Edinburgh Inventory (Oldfield, 1971). They had normal orcorrected-to-normal visual acuity in both eyes and were naïve as to the purposes ofthe experiment. Exclusion criteria were injuries to the hands or their innervationsand dyslexia, that it is known to be associated with tactile impairments (Grant,Zangaladze, Thiagarajah, & Sathian, 1999). The procedures were approved by theEthical Committee of the “G. d’Annunzio” University, Chieti and were in accordancewith the ethical standards of the 1964 Declaration of Helsinki.

2.2. Apparatus

All images were collected with a 1.5 T Siemens Magneton Vision scanner witha standard head coil operating at the “Istituto di Tecnologie Avanzate Biomediche”(ITAB; Chieti, Italy). Participants lay supine in the scanner with the arms outstretchedbeside the abdomen. Foam rubber fixed on the abdomen was used to reduce tactilesensation due to the stimulus weight during the haptic exploration run. A mirrorpositioned above the subject’s eyes provided unobstructed visualization of imagesprojected onto a screen at the rear magnet aperture. Head restraint straps and foamwere utilized to minimize head movement. Sound-attenuating headphones wereused to muffle scanner noise and also served to convey verbal instructions (seebelow). The sequence and timing of the stimuli in all runs were controlled by a PC-compatible computer running Cogent 2000 (developed by the Cogent 2000 team atthe FIL and the ICN; available at http://www.vislab.ucl.ac.uk) and Cogent Graphics(developed by John Romaya at the LON at the Wellcome Department of Imaging Neu-roscience; available at http://www.vislab.ucl.ac.uk) under Matlab (The MathWorksInc., MA, USA).

2.3. Stimuli and procedure

Functional MR images were collected using a gradient-echo echo-planar imag-ing (EPI) sequence. Each subject underwent four functional acquisition scans, duringwhich he/she performed the visual perception, haptic exploration, haptic imagery,and visual imagery task, respectively. The order of the functional scans was coun-terbalanced across subjects. Each experimental scan included 117 consecutivevolumes, but the visual stimulation scan included 69 volumes. Each volume com-prised 28 consecutive 4-mm thick slices oriented parallel to the anterior–posteriorcommissure plane and covering the whole brain (TR = 3.1 s, TE = 60 ms, 64 × 64image matrix, 4 mm × 4 mm in-plane resolution). T1-weighted anatomical imageswere collected using multiplanar rapid acquisition gradient echo sequence (1 mmisotropic voxels, 160 sagittal slices, TR = 11.4 ms, TE = 4.4 ms).

2.3.1. Visual perception taskThe task consisted in passive observation of visual stimuli. Stimuli were the

same as those used in previous studies to functionally localize EBA (Downing, Jiang,Shuman, & Kanwisher, 2001). The stimuli were grey-scale photographs depictingbody-parts and object-parts on a uniform background, presented for 300 ms andfollowed by a fixation-only interval of 500 ms. Twenty stimuli for each categorywere used. The acquisition scan consisted of four alternations of 16-s body, objectand fixation-only blocks, with an additional fixation-only block at the beginning ofthe run.

2.3.2. Haptic exploration taskParticipants were required to haptically explore and recognize the stimuli. Hap-

tic stimuli were fake real-size polyurethane body parts and real objects (Fig. 1). Fakebody parts were: right and left hands, arms, legs and feet. Real objects were: scissors,bottle, phone receiver, table-tennis bat, colander, cookware, bucket, and hanger. Inkeeping with a previous study of haptic exploration of body parts and objects (Kitadaet al., 2009), we used whole objects rather than object parts since partial presen-tation of objects may not allow their accurate recognition in the haptic modality.

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tions, convolved with a canonical hemodynamic response function. These models

ig. 1. Examples of the body part and object stimuli used during the haptic explo-ation task.

urthermore, the status of body parts in the context of the whole body configu-ation may be different from that of incomplete artifacts (e.g., half a hammer), andore similar to that of complete parts of complex objects (e.g., the receiver of a desk

hone). Indeed, each body part may be represented as having its own function andonceptual properties independently from other body parts. Although we could notefinitely rule out that presenting whole versus partial stimuli may trigger the usef different processing strategies, previous studies have shown that the initial pro-essing of objects in the haptic modality is feature-based (Kilgour & Lederman, 2006;akatos & Marks, 1999), thus suggesting that, within the exploration time windowsed in the present study, both object and body part stimuli were discriminatedsing a local processing strategy.

One exemplar for each stimulus category was presented. Therefore, our hapticxploration task involved the categorization of the stimulus rather than the fine,ithin-category identification of specific body parts or objects as requested in pre-

ious neuroimaging investigation of haptic body perception (Kitada et al., 2009). Anxperimenter placed the stimuli on the subject’s abdomen, which was covered withoam rubber in order to reduce sensation due to the stimulus weight. During each

lock subjects explored two stimuli, each for 8 s. A 4-s rest period allowed the exper-

menter to replace the stimulus with the following one of the same category. Theest between blocks lasted 8 s. The stimulus presentation duration was chosen on theasis of a preliminary experiment conducted on 10 participants (mean age: 21 years;females) who did not take part in the main experiment. This preliminary experi-

ologia 49 (2011) 821–829 823

ment showed that haptic recognition of body part and object stimuli was performedat comparable speed (mean ± S.D.: body parts = 5.12 ± 1.4 s; objects = 5.13 ± 3.3 s;t9 = 0.01, P = 0.993). This result confirms the comparable difficulty of haptic explo-ration of body parts and objects and suggests that any between-stimuli modulationof neural activity cannot be ascribed to task difficulty.

During the haptic acquisition scan, subjects had to keep their eyes closed. “Start”and “stop” verbal instructions indicated subjects to begin or stop exploring biman-ually the experimental stimulus. After each “stop” instruction, the experimenterreplaced the stimulus with the next one. During this time, the subjects held theirhands beside the abdomen so as not to interfere with stimulus replacement. Theinstructions were provided by means of headphones to both the participant andthe experimenter. Before beginning the experiment, participants were instructednot to pick up the stimuli during exploration. Subjects wore latex gloves to mini-mize tactile sensation. Thus, processing of the stimuli involved only perception andrecognition of their shape and not of their surface features.

2.3.3. Visual imagery taskIn the visual imagery task, participants were required to create a visual image of

the stimulus cued by audio-recorded words that were presented to the participantsby means of headphones. In separate blocks, the words could represent the bodyparts or the objects used in the haptic exploration task. Each run consisted of sixexperimental blocks for each category (body parts; objects). Each block lasted 20 swith 8-s rest periods between blocks. During each block subjects imagined fourstimuli, each for 4 s, with a 4-s rest period intervening every two stimuli. A “stop”instruction indicated the beginning of the rest period. Thus the timing of the imagerytask was comparable to that of the haptic exploration task. Participants kept theireyes closed during the imagery runs.

2.3.4. Haptic imagery taskIn the haptic imagery task, participants were required to imagine to hapti-

cally explore the cued stimulus avoiding any visual image. Stimulation, timing andimaging procedures were identical to the visual imagery task.

2.4. Statistical analysis

fMRI data were analyzed using SPM8 (Wellcome Department of Cognitive Neu-rology, Institute of Neurology, London) according to the following procedure. Foreach subject, functional images were first corrected for head movements usinga least-squares approach and six-parameter rigid body spatial transformations(Friston et al., 1995). The high-resolution anatomical image and the functionalimages were then stereotactically normalized to the Montreal Neurological Insti-tute (MNI) brain template used in SPM8 (Mazziotta, Toga, Evans, Fox, & Lancaster,1995). Functional images were resampled with a voxel size of 3 mm × 3 mm × 3 mmand spatially smoothed with a three-dimensional Gaussian filter of 8 mm full widthat half maximum to accommodate anatomical variations between subjects (Fristonet al., 1995).

2.4.1. Visual perception scanThe time series of functional MR images obtained from each participant during

the visual perception run was analyzed separately. The effects of the visual per-ception scan were estimated on a voxel-by-voxel basis using the principles of thegeneral linear model extended to allow the analysis of fMRI data as a time series(Worsley & Friston, 1995). Each experimental block was modeled using a boxcar,convolved with a canonical hemodynamic response function, chosen to representthe relationship between neuronal activation and blood flow changes. For eachsubject-specific model, linear compounds of the regression parameter estimates(i.e. linear contrasts) were used to estimate the size of the effects of interest, that is,higher activity while observing body parts than objects. Thus, for each subject weobtained a statistical parametric map of the t statistics, representing all the voxelsmore activated during the visual perception of body parts compared to the visualperception of objects. Clusters of more than ten adjacent voxels surviving a thresh-old of P < 0.05, corrected for multiple comparisons using false discovery rate (FDR),were formed. Localization and visualization of individual activations by SPM wereachieved using BrainShow, in-house software (code by G. Galati) for visualization offMRI data, allowing superimposition of individual SPM maps on cortical surface ofthe single-subject MNI canonical brain (Colin27).

2.4.2. Haptic exploration, haptic imagery and visual imagery scansFor each participant and for each region identified in the visual perception

scan, we first computed an averaged time course for the haptic exploration, hapticimagery, and visual imagery scans, by averaging spatially normalized, unsmoothedtime courses across all the voxels within that region. The effects of the experimentalparadigm were estimated on such averaged time courses through subject-specificgeneral linear models, where experimental blocks were modeled using box-car func-

yielded six parameter estimates for each region and subject, representing the esti-mated amplitude of the hemodynamic response in the six experimental conditions(haptic exploration of body parts and objects, haptic imagery of body parts andobjects, and visual imagery of body parts and objects) relative to the baseline. Theseaverage regional response estimates were entered into a group repeated-measures

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Fig. 2. Activation profile of right and left extrastriate body area (EBA) and right fusiform body area (FBA). The left panel shows the areas localized comparing the visualp one os thee erpretw

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resentation of body and object stimuli (voxels that were labeled as EBA in at leasthowing a body selective response in each voxel. The graphs in the right panel showxploration, visual and haptic imagery of body parts and objects. *P < 0.05. (For inteb version of this article.)

NOVA, with Region (left EBA, right EBA and right FBA), Modality (haptic explo-ation, haptic imagery and visual imagery) and Stimulus Category (body parts andbjects) as main factors. The Duncan test was used for post hoc pair-wise compar-sons.

Finally, we looked for differential effects outside the regions defined in the visualerception scan, performing a whole-brain analysis with a statistical threshold of< 0.001, uncorrected for multiple comparisons and a minimum cluster size of 15onsecutive voxels. To test for the effect of body selectivity during haptic explo-ation, haptic imagery and visual imagery, we performed the following two-tailedontrasts: (i) haptic exploration of body parts versus haptic exploration of objects;ii) haptic imagery of body parts versus haptic imagery of objects, and (iii) visualmagery of body parts versus visual imagery of objects.

. Results

The subjective reports collected at the end of the fMRI scan-ing session showed that all participants could easily recognizehe stimuli both in the visual and in the haptic modality, confirminghe results of the preliminary behavioral experiment. Furthermore,rompt and clear images of both body parts and objects wereeported in the visual and haptic imagery conditions, suggestinghat all participants could easily comply with the imagery tasknstructions.

.1. Visual perception scan

From single subject analysis of functional magnetic resonancemages, we identified in 12 out of 13 subjects, three different cor-

f the subjects). The colour scale indicates the number of participants (from 1 to 12)percentage BOLD signal change (mean ± s.e.m.) of the three ROIs during the haptication of the references to colour in this figure legend, the reader is referred to the

tical regions where the BOLD signal was significantly differentduring observation of body parts compared with the observationof objects. The locations of the three regions corresponded to theleft and right EBA and to the right FBA. The mean MNI coordinatesof the peak of activation in the left and right EBA were −51 (±6.6);−70 (±5.4); 11 (±6.6) and 54 (±5.5); −64 (±8.4); 1 (±7.7), respec-tively. The peak of activation in the right FBA was 43 (±3.9); −45(±7.2); −26 (±3.1) (Fig. 2). Moreover, in four out of 13 participantswe also found a cluster centered on the right inferior frontal gyrus(mean MNI coordinates 42 (±3.3); 15 (±6.1); 24 (±4.2)). However,being present only in a limited number of subjects, this cluster wasnot further considered.

3.2. Haptic exploration, haptic imagery and visual imagery scans

A group repeated-measures ANOVA, with Region (left EBA,right EBA and right FBA), Modality (haptic exploration, hapticimagery and visual imagery) and Stimulus Category (body partsand objects) as main factors was conducted. The main effects ofRegion [F(2,22) < 1] and Stimulus Category [F(1,11) = 2.32; P = 0.156]

were non significant. The non significant effects of Modality[F(2,22) = 1.09; P = 0.354] and of the interaction between Regionand Modality [F(4,44) < 1] suggest the absence of any overall dif-ference between the neural activation of the three areas duringthe haptic exploration and the visual and haptic imagery tasks.

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Table 1MNI coordinates of peaks of relative activation when comparing: (a) haptic explo-ration of body parts versus haptic exploration of objects and (b) visual imagery ofbody parts versus visual imagery of objects.

Anatomical description MNI coordinates

Side x y z Z-score

(a) Haptic bodyMiddle occipital gyrus R 42 −84 18 4.14Inferior parietal lobule R 54 −54 51 3.66Inferior frontal gyrus R 48 36 24 3.48(b) Visual imagery bodyMiddle occipital gyrus R 33 −75 27 3.36Inferior temporal gyrus R 57 −63 −9 3.63

M. Costantini et al. / Neuro

he interaction between Modality and Stimulus Category wason significant [F(2,22) = 1.49; P = 0.246]. However, a significantegion by Stimulus Category [F(2,22) = 5.79; P = 0.001] interac-ion suggested a different degree of body-selectivity in the threereas across tasks. The interaction was explained by higher BOLDesponse for body parts as compared to objects in both left andight EBA (BOLD signal change, mean ± s.e.m.: left EBA: body parts:.08 ± 0.2; objects: −0.15 ± 0.22; P = 0.007; right EBA: body parts:.03 ± 0.13, objects: −0.18 ± 0.14; P = 0.015), but not in right FBAbody parts: −0.05 ± 0.16; objects: 0.02 ± 0.15; P = 0.285). Inter-stingly, the tree-way interaction between Region, Modality andtimulus Category was also significant [F(4,44) = 3.1; P = 0.023;ig. 2]. Post hoc comparisons showed that activation in both theeft and the right EBA was stronger for haptic exploration of bodyarts than of objects (left EBA: body parts: 0.26 ± 0.57; objects:0.08 ± 0.58, P = 0.023; right EBA: body parts: 0.34 ± 0.34; objects:.02 ± 0.37; P = 0.031). In contrast, right FBA did not show any bodyelectivity for the haptic exploration, being in fact more activatedy haptic exploration of objects (BOLD signal change: 0.36 ± 0.34)han by haptic exploration of body parts (BOLD signal change:.03 ± 0.27; P = 0.023). Moreover, only in left EBA visual imageryf body parts produced stronger activation as compared to visualmagery of objects (body parts: 0.23 ± 0.18; objects: −0.08 ± 0.13;= 0.036). No significant difference was observed in any areasetween the haptic imagery of body parts and objects (all Ps > 0.2).hen comparing the activation of each region across tasks for each

timulus category, we found the following: BOLD signal changes ofeft EBA during haptic exploration and visual imagery were compa-able for body parts (P = 0.813) and objects (P = 0.974). In contrast,ight EBA was more activated during haptic exploration than dur-ng visual imagery of body parts (P = 0.001), while no difference

as observed for objects (P = 0.192). On the other hand, activa-ion of right FBA was comparably low during haptic explorationnd visual imagery of body parts (P = 0.834), while it was greateruring haptic exploration than during visual imagery of objectsP < 0.001). When comparing the body-related activity in each taskcross regions we found the following: BOLD signal change dur-ng the haptic exploration of body parts was higher in right EBAompared to FBA (P = 0.03) and comparable to left EBA (P = 0.541),hich in turn tended to be different from that in FBA (P = 0.094).oreover, BOLD signal change during visual imagery of body partsas higher in left EBA compared to both right EBA (P = 0.05) and FBA

P = 0.013), which in turn did not differ from each other (P = 0.498).uring the haptic imagery of body parts no modulation was foundcross regions (all Ps > 0.18).

To further specify the pattern of body selectivity of left and rightBA during haptic exploration and visual imagery, we comparedpaired t-test, two-tailed) for each region and across condition aody-selectivity index calculated as the difference between BOLDignal change for haptic perception or visual imagery of bodyarts and haptic perception or visual imagery of objects. No dif-erence was observed between the body-selectivity indices duringaptic exploration and visual imagery for both left [0.34 ± 0.1 vs..31 ± 0.16; t(11) = 0.138, P = 0.893] and right EBA [0.32 ± 0.11 vs..13 ± 0.17; t(11) = 0.963, P = 0.356], thus showing a comparableody selectivity of EBA activation during haptic perception andisual imagery.

The whole-brain analysis comparing responses to body partsersus objects in the three modalities revealed other body selec-ive cortical areas (see Fig. 3). In particular, when testing for bodyelectivity during the haptic exploration scan, we found only right

emisphere activations involving the middle occipital gyrus, infe-ior parietal lobule, and inferior frontal gyrus (Table 1a). That thehole-brain analysis did not disclose any haptic body activation

n the left occipito-temporal cortex may be due to the small spatialxtent of body-selective activations which may vary across subjects

Calcarine cortex R 21 −60 18 3.56Inferior parietal lobule L −30 −48 54 3.81Supramarginal gyrus R 60 −27 48 3.51

and mask group effects (see also Kitada et al., 2009). When test-ing for body selectivity during the haptic imagery scan, no voxelsturned out to be significant. Finally, when testing for body selectiv-ity during the visual imagery scan, we found activations in the rightmiddle occipital gyrus and the right calcarine cortex, the right infe-rior temporal gyrus, the left inferior parietal lobule and the rightsupramarginal gyrus (Table 1b).

4. Discussion

The present study was aimed at testing the pattern of activationof lateral and medial occipito-temporal areas involved in the visualprocessing of human body forms during the haptic exploration ofbody parts. To this aim we functionally localized left and right EBAand right FBA as the voxels in the occipito-temporal cortex display-ing higher activation to visual presentation of bodies than objectsand then tested their body selectivity in the other modalities. Wefound that both left and right EBA were activated more by hapticexploration of body parts than of objects. In contrast right FBA didnot show any body selectivity in the haptic modality. Furthermore,both left and right EBA presented a body-selective response duringvisual imagery; however, the response of left EBA to body parts wascomparable during haptic exploration and visual imagery, whereasright EBA was more activated during haptic exploration than visualimagery of body parts.

4.1. EBA activation during haptic processing of the body

The selective activation of EBA during the haptic explorationof body parts clearly shows that body selectivity in EBA is notrestricted to the visual modality but extends to haptic processing.Previous studies have shown that haptic exploration of externalobjects does not engage only sensorimotor and parietal areas butalso the extrastriate visual cortex involved in the visual coding ofobject forms (Amedi et al., 2001, 2002; Pietrini et al., 2004). That theactivation of EBA during haptic exploration was selective for bodystimuli rules out that the observed response may be ascribed to thenon specific activation of object (Grill-Spector et al., 2001; Malachet al., 1995) or motion (Tootell et al., 1995; Zeki et al., 1991) selec-tive areas that are adjacent to EBA. Crucially, the activation of theextrastriate cortex during haptic object exploration resembles thecategory-selective pattern observed for the visual modality (Kitadaet al., 2009; Pietrini et al., 2004). In particular, the haptic explo-ration of faces and body parts activates FFA and EBA, respectively

(James et al., 2006; Kilgour et al., 2005; Kitada et al., 2009), whichare selectively involved in the visual processing of the same stim-ulus categories (Downing et al., 2001; Gauthier et al., 2000; Haxbyet al., 2000; Kanwisher et al., 1997; Kitada et al., 2009).

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826 M. Costantini et al. / Neuropsychologia 49 (2011) 821–829

Fig. 3. Results of the whole-brain analysis comparing body parts and object stimuli in the haptic perception (red) and visual imagery (green) tasks. The yellow indicates thea ercepta of theo

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reas of spatial overlap between the body-selective activations during the haptic ps right extrastriate body area (rEBA) in at least one participant. (For interpretationf this article.)

In keeping with previous studies, the present result points tohe existence of a multimodal representation of objects, faces andodies in the human extrastriate cortex. Note that previous stud-

es of category selectivity during haptic perception (James et al.,006; Peelen & Downing, 2007; Pietrini et al., 2004) required ane-grained identification among different exemplars belongingo the same category (e.g., different individual faces, hands or feet),task that may have triggered per se the access to a visual repre-

entation of the explored body part. In contrast, we used a simpleategorization task, requiring the discrimination between differentypes of body parts (e.g., hand vs. foot), ruling out that EBA activa-ion in the haptic modality is dependent on the complexity of thedentification task. Thus, the present results document the involve-

ent of EBA in the detection of body specific features during hapticrocessing (Hodzic et al., 2009).

The whole-brain analysis allowed us to specify the spatial over-ap between body selective areas activated in the visual and haptic

odalities. We found a greater response to haptic exploration ofody parts as compared to objects in the right, but not left, middleccipital cortex. That the activation of the left occipito-temporalortex corresponding to left EBA was not disclosed by the grouphole-brain analysis may be due to the small spatial extent of body-

elective activations which may vary across subjects (see Kitada etl., 2009, for a similar effect). In a similar vein, the body-selectiveaptic region in the right occipito-temporal cortex overlapped onlyith the more posterior and dorsal part of EBA. The spatial sep-

ration between haptic and visual body-selective regions in theccipito-temporal cortex was also suggested by Kitada et al. (2009),uggesting that different groups of largely overlapping populationsf neurons may be involved in the two modalities. However, it isorth noting that differences in the stimuli used in the visual andaptic modalities may have induced a different pattern of acti-ation. In particular, recent studies (Bracci, Ietswaart, Peelen, &avina-Pratesi, 2010; Orlov, Makin, & Zohary, 2010) have suggestedsomatotopic organization of the body-selective activations in theccipito-temporal cortex, with representation of trunk and torsoarts occupying a more ventral and anterior position as comparedo that of upper and lower limbs, respectively. Since the visual EBAocalizer scan included whole body stimuli, in which arms, legs andorsos of human bodies were presented, while only limbs were pre-

ented in the haptic exploration scan, the different spatial extentnd position of visual and haptic body-selective areas may reflecthe activation of true multimodal population of neurons respondingo different body parts.

ion and visual imagery tasks. The black line outlines the location of voxels labeledreferences to colour in this figure legend, the reader is referred to the web version

4.2. Multimodal recognition of body forms in EBA

Behavioral studies have shown that humans are able to extractimportant information from haptic perception of objects, faces andbody parts. In a series of studies Kaitz and colleagues requiredblindfolded participants to identify, among three alternatives, theirpartners (Kaitz, 1992) or newborn infants (Kaitz et al., 1993, 1994)by haptic exploration. They found that both men and women,although with different accuracy levels, were able to recognizefamiliar individuals by only touching the dorsum of the hand. Themost salient features used for recognition were the material prop-erties of the skin, like the presence of hair for recognition of thepartner, and the texture and temperature for infant recognition. Inthe present study, we asked participants to wear latex glove dur-ing haptic exploration. This was aimed at reducing the perceptionof material cues and isolating the effect of shape perception. Thus,haptic recognition of body parts was arguably based on processingthe body shape.

The neural representation of tactile processing of material andgeometrical shape information are segregated as early as in pri-mary somatosensory cortex (Bodegård, Geyer, Grefkes, Zilles, &Roland, 2001). Beyond the primary cortex, the hierarchical flowof somatosensory information seems to involve the secondarysomatosensory cortex for the processing of material informationand the anterior part of the intraparietal sulcus area (aIPS) forthe processing of objects’ shape (James, Kim, & Fisher, 2007;Roland, O’Sullivan, & Kawashima, 1998). Crucially, aIPS receivesmultimodal signals from motor (Binkofski, Buccino, Posse, et al.,1999; Binkofski, Buccino, Stephan, et al., 1999) and visual systems(Grefkes, Weiss, Zilles, & Fink, 2002; Zhang et al., 2004). On theother hand, the involvement of LOC has been consistently demon-strated only in the haptic processing of object shape (James et al.,2007). Thus, aIPS and LOC may provide a multimodal representa-tion of the objects’ shape, with aIPS mainly involved in the guidanceof motor actions and LOC mainly involved in object recognition(James et al., 2002, 2007; Reed, Shoham, & Halgren, 2004). Theseparation of functions between the different areas activated byhaptic processing of objects is analogous and partially overlaps withthe dual-route model proposed in the visual modality (Milner &Goodale, 1995).

In addition to the activation in the right middle occipito-temporal cortex, the whole brain analysis revealed body-selectiveactivations during haptic exploration in the right inferior parietallobe and in the right inferior frontal gyrus. This finding is consistent

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M. Costantini et al. / Neuro

ith the results of the group analysis reported in a previous studyf haptic body perception (Kitada et al., 2009) and may suggesthe existence of different haptic body representations in temporal,arietal and frontal cortices involved in coding form- or action-elated information.

In keeping with the role of LOC in the multimodal recogni-ion of object shape and of FFA in the multimodal recognition oface forms, EBA may be selectively involved in the multimodalecognition of human body forms. Indeed, evidence from the visualodality suggests that EBA is involved in the visual processing of

uman body forms (Peelen & Downing, 2007; Urgesi, Berlucchi, &glioti, 2004;Urgesi, Candidi, Ionta, & Aglioti, 2007). In particular,agnetic stimulation of EBA impairs the visual discrimination of

he form of human body parts, but not of face and object partsUrgesi et al., 2004; Pitcher, Charles, Devlin, Walsh, & Duchaine,009; Urgesi, Candidi, et al., 2007). Furthermore, a recent neuropsy-hological study (Moro et al., 2008) has shown that patients withesions encompassing EBA were impaired in the visual discrimina-ion of body parts but not of face and object parts, thus providingvidence for the existence of body form visual agnosia.

Visual recognition deficits may co-occur with haptic recogni-ion deficits. Neuropsychological studies have provided evidence ofssociated visual and tactile agnosia after occipito-temporal dam-ge (Feinberg, Rothi, & Heilman, 1986; Morin, Rivrain, Eustache,ambert, & Courtheoux, 1984; Ohtake et al., 2001). In a similarein, it has been reported the case of a prosopoagnosic patient whoas unable to recognize faces in the visual as well as in the hapticodality (Kilgour et al., 2004). Importantly, the patient was unim-

aired in the haptic discrimination of objects, thus indicating thathe category-selective extrastriate infero-temporal cortex housesmultimodal representation of faces. What remains unknown ishether selective deficits in the visual discrimination of human

ody parts co-occur with deficits in haptic perception of body partss compared with face and object parts. This is an important issueo address in future studies.

.3. Configural and local processing in haptic body perception

The activation of EBA, but not of FBA, during haptic explorationf body parts may reflect the complementary roles of lateral andedial occipito-temporal areas in the local and configural process-

ng of body stimuli. Haptic exploration typically implies a localrocessing. This may explain why we found EBA, but not FBA acti-ation during haptic perception of the human body. Indeed, duringaptic exploration we can only perceive small parts of objects,

aces, or body parts, while the entire shape can be fully extractednly by integrating over time the information acquired at differ-nt instants (Kitada, Kochiyama, Hashimoto, Naito, & Matsumura,003; Peelen, Rogers, Wing, Downing, & Bracewell, 2010). Stud-

es on haptic object exploration have shown that object processings feature-based in the initial stages, while a more global repre-entation emerges only when more time is allowed for manualxploration (Lakatos & Marks, 1999). It is worth noting that inver-ion effect for haptic exploration of faces is found when subjectsave no time constraints in exploring the stimulus but not whenhe exploration has to be completed within a time window of0 s (Kilgour & Lederman, 2006). Since participants of the presenttudy could explore the body parts and the objects for only 8 s,t is unlikely that configural processing and FBA were called intoction during the haptic exploration task. Therefore, although weid not find any response of FBA during brief haptic exploration of

ody parts, we cannot exclude that FBA may be recruited during

onger exploration of single body parts or of more complex bodyonfigurations which entail configural processing. This would be ineeping with visual body processing studies demonstrating an FBAody selective response for complex body configurations but not

ologia 49 (2011) 821–829 827

for single body parts (Taylor et al., 2007). The specific involvementof FBA in configural processing as compared to the involvementof EBA in local processing of the human body (Taylor et al., 2007;Urgesi, Calvo-Merino, et al., 2007) is also functionally and anatomi-cally analogue to the respective role of FFA and OFA in the configuraland local processing of faces (Haxby et al., 2000; Yovel & Kanwisher,2005). In a similar vein, the differential role of medial and lateraloccipito-temporal areas in configural and local processing mightalso explain the higher response of FBA to the haptic explorationof objects with respect to single body parts. Indeed, this effect mayreflect the response of non selective object-recognition neurons tocomplex configuration of stimuli. Future studies comparing hapticexploration of single and complex arrangements of body and objectparts are needed to better specify the multimodal representation ofthe human body in the medial and lateral occipito-temporal cortex.

4.4. Visual imagery of human body parts

The activation of EBA during haptic body perception is notlikely to be entirely due to visual mediation, i.e. to the transla-tion of haptic input into visual images processed by visual areas(Kilgour & Lederman, 2002; Lederman et al., 1990; Zhang et al.,2004). Behavioral evidence for the use of visual mediation duringhaptic processing has been provided for objects (Lederman et al.,1990) but not for faces (Kilgour & Lederman, 2002). The activation ofvisual cortex during haptic exploration may reflect, at least in part,the visual imagery of the touched objects (Sathian & Zangaladze,2002; Zhang et al., 2004). However, the fact that LOC activity ishigher during haptic perception than during visual imagery (Amediet al., 2001) and is present also in congenitally blind individu-als (Mahon, Anzellotti, Schwarzbach, Zampini, & Caramazza, 2009;Pietrini et al., 2004) would support the notion that the extrastriatevisual cortex houses a true multisensory representation of objects(Zhang et al., 2004). Furthermore, during haptic exploration of unfa-miliar and familiar objects, the extrastriate cortices are influencedby the somatosensory cortex (likely mediating bottom-up influ-ences of somatic inputs on multimodal representations) and byposterior parietal, premotor, and prefrontal cortices (likely mediat-ing top-down control over visual imagery) (Deshpande, Hu, Lacey,Stilla, & Sathian, 2010; Deshpande, Hu, Stilla, & Sathian, 2008). Wecannot rule out that participants used visual mediation during thehaptic exploration task or that the involvement of EBA during hap-tic exploration of the body may be partially due to visual imagery.Indeed, both left and right EBA showed a comparable degree of bodyselectivity during haptic exploration and visual imagery. However,the use of visual imagery may have a different influence on theactivation of left and right EBA during haptic exploration of humanbody parts. Since we found that activation of right EBA was higherduring haptic exploration of body parts than during visual imageryof body parts, we can exclude that visual mediation per se was theonly cause of the response of right EBA during haptic processingof body parts. Thus, in keeping with previous studies on objecthaptic perception (Amedi et al., 2001), the multimodal represen-tation of the body in right EBA may be partially independent fromvisual imagery. On the other hand, left EBA was equally active dur-ing haptic exploration and visual imagery of body parts, pointingto the possibility that the involvement of left EBA during hapticbody exploration may be due to the creation of visual images of theexplored body parts.

The whole-brain analysis revealed a number of occipital, tem-poral and parietal areas showing a selective response during visual

imagery of the body. The activation of the right middle occipi-tal gyrus and right inferior temporal gyrus, in a location roughlycorresponding to right EBA, is in keeping with the body selectiveresponse of EBA during visual imagery. Along with studies show-ing that visual imagery of faces activates FFA, this result confirms

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he category selective activations of the extrastriate cortex dur-ng visual imagery (Ishai, Ungerleider, & Haxby, 2000; O’Craven &anwisher, 2000). The activation of the left and right inferior pari-tal cortex during visual imagery of the body is consistent withhe involvement of these areas in the access to a visual struc-ural representation of the human body during visual imageryasks (Corradi-Dell’Acqua, Hesse, Rumiati, & Fink, 2008; Corradi-ell’Acqua, Tomasino, & Fink, 2009).

. Conclusion

The presented study documented differences in the functionalctivation of extrastriate body-selective areas during haptic explo-ation and imagery. Right and left EBA, but not right FBA, wereelectively activated during haptic exploration of human bodyarts, suggesting an involvement in the multimodal perception ofhe human body. Furthermore, both left and right EBA showed aody selective response during visual imagery. However, differentatterns of activation during haptic perception and visual imageryf body parts were found, with right EBA being more activateduring haptic perception than during visual imagery, left EBA com-arably activated during haptic perception and visual imagery, andight FBA not activated during haptic perception or visual imagery.hese results points to the existence of multiple multimodal repre-entations of the body in the extrastriate cortex which are activateduring perception and imagery.

cknowledgements

The study was funded by “Istituto Tecnologie Avanzateiomediche” (ITAB), Fondazione Università “G. d’Annunzio”, Chi-ti, Italy and by the Ministero Università e Ricerca of Italy, Sapienzaniversity of Rome, and Fondazione Santa Lucia, Rome (to S.M.A.).e thank P. Downing for providing the EBA localizer stimuli.

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