Is the whole the sum of its parts? Configural processing of headless bodies in the right fusiform gyrus

doi:10.1016/j.bbr.2014.12.015

Behavioural Brain Research

Volume 281, 15 March 2015, Pages 102-110

https://doi.org/10.1016/j.bbr.2014.12.015 Get rights and content

Highlights

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There is clear evidence that we prefer whole bodies compared to the sum of their parts.
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The preference for whole bodies seems to be associated with activation pattern in the right fusiform body area.
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The preference for whole faces seems to be associated with activation pattern in the right and left fusiform face area.

Abstract

The current study aimed to explore the functional magnetic resonance (fMR)-adaption effect by presenting intact and scrambled headless bodies and faces. This fMR-adaption paradigm allows investigating processing specificity in distinct brain areas by comparing the blood-oxygen-level-dependent (BOLD) signal related to the presentation of same or different pairs of bodies. There is clear evidence that we prefer whole bodies compared to the sum of their parts. This effect refers to a subtype of configural processing termed first-order relational information. The preference for whole bodies seems to be associated with activation pattern in body-sensitive brain regions. However, it remains unclear until now, which cortical area exactly mediates this preference. In the present study, we investigated whether there are neuronal populations that show a selective adaption to whole bodies compared to the sum of their parts. The right fusiform body area (FBA) showed a preference for whole bodies compared to the sum of their parts as the right and left fusiform face area showed a preference for whole faces compared to the sum of their parts. Thus, the present data support the idea that configural body and face processing is mediated by the fusiform gyrus. The current data further support the view that bodies are a special stimulus class with specific characteristics which are processed in body-sensitive brain areas.

Introduction

It is controversial whether human bodies, like human faces, are processed by specialized cortical mechanisms. Functional magnetic resonance imaging (fMRI) studies have demonstrated that faces and bodies are processed in specialized cortical brain regions [1], [2], [3], [4], [5], [6] termed occipital face area (OFA), fusiform face area (FFA), extrastriate body area (EBA) and fusiform body area (FBA). The OFA and EBA are located in the occipital gyrus and process body [1], [7] and face parts [8], [9]. The FFA and FBA are situated in the fusiform gyrus and respond to whole bodies and faces [12], [14].

Like faces, bodies differ from other categories as they are processed configurally. Configural processing is associated with the perception of relations between stimulus features. However, previous studies pointed out that different subtypes of configural processing are necessary for the perception of bodies and faces [10], [11], [13], [15], [16]. Maurer et al. [16] describes three different sub-types of configural processing which might be located on a continuum. First-order relational information is followed by holistic information and second-order relational information. First-order relational information is defined as intact spatial arrangement of stimulus features information. Holistic information refers to the integration of stimulus features into single representation whereas second-order relational information refers to metric distance between single stimulus features. First-order relational information is important for face and body processing while holistic information and second-order relational information are necessary for face but not body processing [13], [16]. There is clear evidence for a preference to process whole bodies compared to the sum of their parts [11]. Behavioral data have shown that the visual perception of intact bodies is better compared to stimulus configurations in which the body parts are scrambled and these differences are processed in the time window of the N170 [11]. Thus, first-order relational information plays a central role in configural body processing. However, little is known on where in the brain first-order relational information of human bodies is processed. Taylor et al. [14] systematically increased the amount of body-related information and observed a gradual increase in the activation of the EBA as well as a step-like activation increase in the FBA. This finding supports the notion that the processing of whole bodies is associated with activation in the fusiform gyrus. A recent study by Brandman and Yovel [10] pointed out that both body-sensitive brain areas (EBA and FBA) prefer whole bodies over the sum of its part. These data support the notion that first-order relational information plays a central role in the processing of human bodies. Furthermore, bodies seem to be represented as integrated representations (whole) rather than part-based. What remains unclear however, are the functional characteristics of the underlying neurons in the body-sensitive brain areas. The observation, that the EBA and FBA prefer whole bodies over the sum of their parts does not necessarily imply that both body-sensitive brain areas show a specific sensitivity for the discrimination of intact or scrambled bodies.

To find out, where in the brain first-order relational information of human bodies is processed we conducted an fMR-adaption study [15], [17] in which we compare the blood-oxygen-level-dependent (BOLD) signal in body-sensitive and face-sensitive brain regions between different and same trials. The adaption-effect is defined as stronger BOLD responses in trials with different compared to same stimuli [18]. This paradigm allows for the investigation of the specificity of brain regions involved in the processing of different stimulus classes. Furthermore, this paradigm enables us to tag neuronal populations in a specific brain region and to explore their specific properties. In accordance with previous studies [19], we manipulated first-order relational information by presenting intact and scrambled bodies (see, Fig. 1). Considering the described similarities between body and face processing mechanisms [10], [11], we decided to use intact and scrambled faces as control stimuli.

Taken together, in the present study, we used an fMR-adaption paradigm to investigate whether there are neuronal populations that show selective adaption to whole bodies compared to the sum of their parts. Therefore, we measured the adaption-effect for intact (whole) and scrambled (sum of their parts) bodies in body-sensitive brain regions (EBA and FBA). We used faces as control stimuli as previous studies demonstrated several similarities between the processing mechanisms and characteristics of bodies and faces [for review, see 13]. Thus, a neuronal correlate for configural body processing would be reflected by selective adaption for whole compared to scrambled bodies.

Section snippets

Participants

Sixteen right-handed subjects (9 male, mean age 23.0 years, SD = 3.0 age range: 20–30 years) participated in the current study. None of the subjects reported a history of neurological or psychiatric illness. All participants had normal or corrected-to normal vision. Written informed consent was obtained from all subjects prior to participation. The study was performed in accordance with the ethical standards laid down in the declaration of Helsinki (Varga, 1975) and was approved by the Ethics

Behavioral data

RTs and accuracy data are illustrated in Fig. 2.

For accuracy data, analysis revealed main effects of Category (F_1,15 = 54.6, p < 0.001) and Presentation Type (F_1,15 = 25.7, p < 0.001) with better performances for faces compared to bodies and for intact compared to scrambled stimuli. Furthermore, there was a significant interaction between Category and Presentation Type (F_1,15 = 27.0, p < 0.001). Subsequent paired comparisons revealed better performances for intact compared to scrambled bodies (T₁₅ = 46.6, p <

Discussion

The current study aimed to explore whether there are neural populations that selectively mediates configural body processing. Configural body processing has been investigated by manipulating first-order relational information. First-order relational information refers to the spatial arrangement of stimulus features and can be disturbed by scrambling an object in distinct parts and displacing the order of these parts (dividing a stimulus in the sum of its parts). Previous studies found a clear

Conclusion

Taken together, the present study shows for the first time that neuronal populations of the right FBA show a preference for whole bodies compared to the sum of their parts as neuronal populations of the right and left FFA showed a preference for whole faces over the sum of their parts. Thus, first-order relational information of bodies and faces might be processed in comparable but distinct brain regions.

Conflict of interest

We disclose any financial or other relationships that could be interpreted as a conflict of interest including those (a) with manufacturer(s) of any commercial products and/or provider(s) of commercial services and (b) with any commercial support of the research reported in the manuscript submitted for publication. There are no other sources of financial support.

Acknowledgments

We would like to thank Lisa Schriewer and Sabine Bierstedt who helped with data collection and stimulus preparation. We also thank Patrizia Thoma for her comments on the manuscript. This work was supported by a grant from the German Research Society (DFG: SU 246/8-1).

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Research reportIs the whole the sum of its parts? Configural processing of headless bodies in the right fusiform gyrus

Highlights

Abstract

Introduction

Section snippets

Participants

Behavioral data

Discussion

Conclusion

Conflict of interest

Acknowledgments

Curr Biol

Curr Biol

Clin Neurophysiol

Neurosci Biobehav Rev

Trends Cogn Sci

Acta Psychol (Amst)

A cortical area selective for visual processing of the human body

Science

The fusiform face area: a module in human extrastriate cortex specialized for face perception

J Neurosci

The fusiform face area: a cortical region specialized for the perception of faces

Philos Trans R Soc Lond B: Biol Sci

Selectivity for the human body in the fusiform gyrus

J Neurophysiol

Research report
Is the whole the sum of its parts? Configural processing of headless bodies in the right fusiform gyrus