Elsevier

NeuroImage

Volume 45, Issue 4, 1 May 2009, Pages 1264-1271
NeuroImage

Distinct cortical networks for the detection and identification of human body

https://doi.org/10.1016/j.neuroimage.2009.01.027Get rights and content

Abstract

In the human brain information about bodies and faces is processed in specialized cortical regions named EBA and FBA (extrastriate and fusiform body area) and OFA and FFA (occipital and fusiform face area), respectively. Here we investigate with functional magnetic resonance imaging (fMRI) the cortical areas responsible for the identification of individual bodies and the distinction between ‘self’ and ‘others’. To this end we presented subjects with images of unfamiliar and familiar bodies and their own body. We identified separate coactivation networks for body-detection (processing body related information), body-identification (processing of information relating to individual bodies) and self-identification (distinction of self from others). Body detection involves the EBA in both hemispheres, and in the right hemisphere: the FBA and areas in the IPL (inferior parietal lobe). Body identification involves areas in the inferior frontal gyrus (IFG) of both hemispheres and in the right hemisphere areas in the medial frontal gyrus (MFG), in the cingulate gyrus (CG), in the central (CS) and the post-central sulcus (PCS), in the inferior parietal lobe (IPL) and the FBA. When the recognition of one's own body is contrasted to the identification of familiar bodies, differential activation is observed in areas of the inferior parietal lobe (IPL) and inferior parietal sulcus (IPS) of the right hemisphere, and in the posterior orbital gyrus (pOrbG) and in the lateral occipital gyrus (LOG) of the left hemisphere. Thus, identification of individual bodies and self-other distinction involve in addition to the classical occipito-parietal network a parieto-frontal network. Interestingly, the EBA shows no differential activation for distinctions between familiar or unfamiliar bodies or recognition of one's own body.

Introduction

Identification and recognition of individuals rely to a large extent on visual information about features of faces and bodies and so do judgments on the emotional state and intentions of the respective others. Accordingly, it is argued that there are areas of the cerebral cortex specialized for the processing of body and face related information. These are the EBA and FBA (extrastriate and fusiform body area) and OFA and FFA (occipital and fusiform face area), respectively (Puce et al., 1996, Kanwisher et al., 1997, Downing et al., 2001, Peelen and Downing, 2005, Schwarzlose et al., 2005, Downing et al., 2006, Peelen et al., 2006). These are the EBA and FBA (extrastriate and fusiform body area) and OFA and FFA (occipital and fusiform face area), respectively (Puce et al., 1996, Kanwisher et al., 1997, Downing et al., 2001, Peelen and Downing, 2005, Schwarzlose et al., 2005, Downing et al., 2006, Peelen et al., 2006).

The first localizations of areas in the human visual cortex responding selectively to images of bodies and body parts have been performed with functional Magnetic Resonance Imaging (fMRI) in humans (Downing et al., 2001) and in monkeys (Pinsk et al., 2005, Tsao et al., 2003), and confirmed with additional methods such as Evoked Potentials (EP) (Kovacs et al., 2005, Thierry et al., 2006), Intracranial Recordings (Pourtois et al., 2007) and Transcranial Magnetic Stimulation (TMS) (Urgesi et al., 2004, Urgesi et al., 2007a, Urgesi et al., 2007b). Single-cell recordings in non-human primates also point to a remarkable functional selectivity of neurons for shapes of bodies and body parts in the inferior temporal cortex (Gross et al., 1972, DeSimone et al., 1984, Wachsmuth et al., 1994, Tsao et al., 2006, Kiani et al., 2007).

However, the notion of distinct, category specific cortical regions is still a matter of debate. There is also evidence that the representations of faces and objects in ventral temporal cortex are widely distributed and overlapping (Haxby et al., 2001, Ishai et al., 2000, O'Toole et al., 2005) and that the specialization of the face selective area is dependent on expertise (Gauthier et al., 1999). Thus, local specialization and distributedness coexist and further investigations are needed to unveil the nature of cortical representations.

Faces and bodies constitute a unique object category because they can be further classified according to identity and ownership. Together with gait, gesture and prosody faces and bodies are crucial for the assessment of a person's identity. Visual information extractable from faces and bodies allows for judgments on gender, age, and ethnicity and ultimately the identity of a person. This includes as special case the identification of a body or a face as belonging to oneself or someone else.

The distinction between self and other and the representation of the self rely on numerous sources of information. Proprioceptive and visual signals contribute to the representation of the dynamic body scheme and the awareness of ownership of the body (Jackson and Decety, 2004, Uher et al., 2005, Pellijeff et al., 2006, Shimada et al., 2005, Vogeley et al., 2001). Furthermore, investigations of the sense of agency revealed differential cortical activation patterns for the anticipation, visualization, and observation of one's own movement versus that of others (Chaminade and Decety, 2002, Cunnington et al., 2006, Grezes et al., 2004, Ramnani and Miall, 2004). Because of the prominent role of facial cues for the discrimination of an person's identity the studies on self-representation and self vs. others distinction are based on the distinction between one's own face and that of others (Platek et al., 2006, Uddin et al., 2005, Uddin et al., 2006). In the present study we investigated networks involved in self-other distinction that rely on non-facial cues. To this end we presented images of headless bodies and examined whether self-body-identification is reflected in the differential activation of the cortical areas involved in the encoding of bodies or body parts (EBA and FBA) or whether it involves in addition specific networks devoted to the distinction between self and other in a more general sense.

We examined subjects with event related fMRI while they performed two explicit two-alternative, forced-choice identification tasks: 1. distinction of one's own body from other unfamiliar bodies and 2. distinction of a familiar body from other unfamiliar bodies. This paradigm was used in order to dissociate ‘familiarity’ from the distinction between ‘self’ and ‘other’. In a previous study, based on a block design and passive viewing conditions, we found that cortical areas responding to bodies and self-other distinctions were not restricted to the extrastriate visual cortex (Hodzic et al., 2008). In the current study, we applied a block design to identify body related areas and an event related design for the segregation of areas involved in the self-other distinction, manipulating the identity, familiarity and the viewpoint of the presented body images.

Section snippets

Methods

Ten human volunteers (mean age 27 years, 5 females) with normal or corrected-to-normal vision took part in this study. All participants gave their informed written consent to the procedure in accordance with institutional guidelines and the Helsinki declaration (www.wma.net/e/ethicsunit/helsinki.htm).

For the compilation of the stimulus material subjects wearing dark blue bikinis or swimming suits were photographed in neutral, frontal, upright posture against a non-reflecting gray background.

Behavioural measures

The reaction times (RT) and accuracy of the responses during the identification experiments were as follows: condition ‘self’; RT = 1027 ms, 98% correct, condition ‘familiar other’; RT = 1029 ms, 95% correct, condition ‘other 1’ (other in ‘self’ run); RT = 1032 ms, 98% correct, and condition ‘other 2’ (other in ‘familiar other’ run); RT = 1030 ms, 99% correct (Fig. 1).

Repeated measures ANOVA revealed that the accuracy for the condition ‘familiar other’ was significantly lower than for the condition

Discussion

The goal of this study was to differentiate between cortical areas devoted to the analysis of body related information: 1.) the processing of visual, body specific features (body-detection), 2.) the distinction between familiar and unfamiliar bodies (body-identification) and 3.) the distinction of one's own body (self-identification).

Acknowledgment

We are grateful to S. Weigelt for contributions to experimental design and data analysis.

References (60)

  • PourtoisG. et al.

    Direct intracranial recording of body-selective responses in human extrastriate visual cortex

    Neuropsychologia

    (2007)
  • SakataH. et al.

    Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey

    Brain Res

    (1973)
  • SaxeR. et al.

    Divide and conquer: a defense of functional localizers

    Neuroimage

    (2006)
  • ShimadaS. et al.

    The parietal role in the sense of self-ownership with temporal discrepancy between visual and proprioceptive feedbacks

    Neuroimage

    (2005)
  • SugiuraM. et al.

    Cortical mechanisms of visual self-perception

    Neuroimage

    (2005)
  • SugiuraM. et al.

    Multiple brain networks for visual self-recognition with different sensitivity for motion and body part

    Neuroimage

    (2006)
  • ThierryG. et al.

    An event-related potential component sensitive to images of the human body

    Neuroimage

    (2006)
  • UddinL.Q. et al.

    Self-face recognition activates a frontoparietal mirror network in the right hemisphere: an event-related fMRI study

    NeuroImage

    (2005)
  • UherR. et al.

    Functional neuroanatomy of body shape perception in healthy and eating-disordered women

    Biol. Psychiatry

    (2005)
  • UrgesiC. et al.

    Magnetic stimulation of extrastriate body area impairs visual processing of nonfacial body parts

    Curr. Biol.

    (2004)
  • VogeleyK. et al.

    Mind reading: Neural mechanisms of theory of mind and self-perspective

    Neuroimage

    (2001)
  • ChaminadeT. et al.

    Leader or follower? Involvement of the inferior parietal lobule in agency

    Neuroreport

    (2002)
  • ChanA.W. et al.

    The effect of viewpoint on body representation in the extrastriate body area

    Neuroreport

    (2004)
  • DaleA.M. et al.

    Selective averaging of rapidly presented individual trials using fMRI

    Hum Brain Mapping

    (1997)
  • DeSimoneR. et al.

    Stimulus-selective properties of inferior temporal neurons in the macaque

    J. Neurosci.

    (1984)
  • DowningP.E. et al.

    A cortical area selective for visual processing of the human body

    Science

    (2001)
  • DowningP.E. et al.

    Domain specificity in visual cortex

    Cereb. cortex

    (2006)
  • EhrssonH.H. et al.

    Neural substrate of body size: Illusory feeling of shrinking of the waist

    PLoS Biol

    (2005)
  • FormanS.D. et al.

    Improved assessment of significant activation in functional magnetic-resonance-imaging (fMRI) - Use of a cluster-size threshold

    Magn Reson Med

    (1995)
  • GauthierI. et al.

    Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects

    Nat. Neurosci.

    (1999)
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