Elsevier

Neuropsychologia

Volume 44, Issue 7, 2006, Pages 1145-1158
Neuropsychologia

Cortical correlates of face and scene inversion: A comparison

https://doi.org/10.1016/j.neuropsychologia.2005.10.009Get rights and content

Abstract

Face recognition is more strongly impaired by stimulus inversion than nonface object recognition. This phenomenon, known as the face inversion effect (FIE), suggests that the visual system contains specialized processing mechanisms that are more engaged by upright faces than by inverted faces or nonface objects. Neuroimaging and neuropsychological studies indicate that environmental scenes may also recruit specialized-purpose processing machinery but a comparable inversion effect for scenes has not been established. Here we demonstrate that both face and scene inversion lead to behavioral penalties during performance of a continuous visual matching task; however, the scene inversion effect was less robust and declined in magnitude over the course of the experiment. Scene inversion led to greater neural response in the functionally defined lateral occipital (LO) object area for inverted versus upright scenes and reduced response in the parahippocampal place area (PPA), while face inversion lead to greater response in LO and the right middle fusiform (MF) object area for inverted versus upright faces but no change in the fusiform face area (FFA). A whole-brain analysis revealed several regions that responded more strongly to either upright versus inverted faces or upright versus inverted scenes, some of which may be involved in post-recognition processing. These results demonstrate that both face and scene inversion cause a shift from specialized processing streams towards generic object-processing mechanisms; however, this shift only leads to a reliable behavioral penalty in the case of face inversion.

Introduction

Many kinds of objects are more difficult to recognize when they are upside-down than when they are in their canonical orientation. Behavioral studies have demonstrated that this inversion penalty is often stronger for faces than for other stimulus categories (Valentine, 1988, Yin, 1969). This phenomenon – known as the face inversion effect (FIE) – has been taken as support for the claim that faces and nonface objects recruit different processing streams (Farah, Wilson, Drain, & Tanaka, 1998). In particular, face recognition is believed to rely more than nonface recognition on configural or holistic information (Carey & Diamond, 1977; Farah, Tanaka, & Drain, 1995; Maurer, Grand, & Mondloch, 2002; Rhodes, Brake, & Atkinson, 1993). Recent studies have demonstrated that inversion impairs the ability to detect the configural aspects of faces (such as the distance between the two eyes) but not individual faces features (such as the color or shape of the eyes) (Bartlett & Searcy, 1993; Freire, Lee, & Symons, 2000; Searcy & Bartlett, 1996). There is evidence that similar configural or holistic processing mechanisms might be recruited by other object categories for which we have extensive expertise and are also more difficult to recognize after inversion (Diamond & Carey, 1986; Gauthier & Tarr, 2002; Rossion & Gauthier, 2002).

Claims for specialized processing streams have also been made for scenes (Aguirre, Zarahn, & D’Esposito, 1998; Epstein, 2005; Epstein & Kanwisher, 1998) and bodies (Downing, Jiang, Shuman, & Kanwisher, 2001). Faces, scenes, and bodies differentially activate specific regions of cortex that tend to be found in the same location across subjects (Kanwisher, 2004, but see Haxby et al., 2001) and both scene and face perception can be specifically impaired by brain damage (Aguirre & D’Esposito, 1999; Epstein, DeYoe, Press, Rosen, & Kanwisher, 2001; Mendez & Cherrier, 2003). Given these claims of specialization, one might expect to find scene and body inversion effects comparable to the FIE. Indeed, a “body-inversion effect” has recently been reported (Reed, Stone, Bozova, & Tanaka, 2003) in which subjects are impaired at discriminating between images of bodies exhibiting different postures when the images are inverted. The magnitude of the body inversion effect was similar to the magnitude of the face inversion effect. In contrast, the few studies that have examined scene inversion reported to have either no effect on recognition performance (Diamond & Carey, 1986; Wright & Roberts, 1996) or a small effect that is significantly less than the FIE (Scapinello & Yarmey, 1970; Yin, 1969).

In the current study, we measure the behavioral effects of face and scene inversion and also use functional magnetic resonance imaging (fMRI) to identify cortical regions that respond differentially to upright versus inverted faces and upright versus inverted scenes. This experiment follows on from a number of earlier studies that examined the effect of inversion on the neural response to faces (Aguirre, Singh, & D’Esposito, 1999; Gauthier, Tarr, Anderson, Skudlarski, & Gore, 1999; Haxby et al., 1999; Kanwisher, Tong, & Nakayama, 1998). Several of these studies focused on the fusiform face area (FFA), a region of cortex that responds much more strongly to faces than to nonface objects and is believed to be critical for face recognition (Kanwisher, McDermott, & Chun, 1997; McCarthy, Puce, Gore, & Allison, 1997; Puce, Allison, Asgari, Gore, & McCarthy, 1996; Rhodes, Byatt, Michie, & Puce, 2004). One might expect that inversion would strongly reduce FFA response to faces. Somewhat surprisingly, these earlier studies indicated that inversion reduces face response in the FFA only mildly (Gauthier et al., 1999, Haxby et al., 1999, Kanwisher et al., 1998; Yovel & Kanwisher, 2004) or not at all (Aguirre et al., 1999). In fact, the greatest effect of face inversion was found in putative “object” areas, which responded more strongly to inverted faces than to upright faces (Aguirre et al., 1999, Haxby et al., 1999). This neural effect was interpreted as reflecting greater engagement of generic object-processing mechanisms to inverted faces. However, a limitation of these earlier studies was the fact that occipitotemporal visual regions were classified as either “face” or “object” areas based on differential response to either faces versus nonface objects (Aguirre et al., 1999) or faces versus houses (Haxby et al., 1999). Thus, these studies did not distinguish between voxels involved in generic processing of objects from voxels that might be preferentially involved in house/scene processing. Furthermore, most of these earlier studies focused on particular regions of interest in occipitotemporal cortex and thus might have overlooked regions outside of these ROIs that responded differentially to upright versus inverted faces. An exception is a study by Leube et al. (2003), which examined effects of face inversion across the whole brain and found greater response to upright than to inverted faces in the right superior temporal sulcus and right insular cortex.

The neural consequences of scene inversion have been comparatively less studied, probably because the behavioral effects of scene inversion have not been reliably established. Haxby et al. (1999) used upright and inverted houses as the nonface comparison stimuli in an fMRI study of the face inversion effect. Although house inversion per se was not a focus of this study, the authors reported reduced response to inverted compared to upright houses in “house-selective” voxels in the medial fusiform part of ventral temporal cortex, but a nonsignficant trend towards greater response for inverted houses in more posterior occipital regions. Insofar as the medial temporal “house-selective” voxels abut the scene-selective parahippocampal place area (PPA; Epstein & Kanwisher, 1998), these results suggest that scene inversion may result in decreased engagement of scene-selective regions but increased engagement of generic object processing regions. In other words, scene inversion and face inversion may have qualitatively similar effects on their respective processing streams. However, in the absence of a nonhouse object comparison condition, it is unclear whether the effects of house inversion in this study are specific to houses, or whether they would apply to a wide variety of stimuli.

In the current study, subjects were scanned while they performed a continuous visual matching task on upright and inverted versions of faces, “scenes” consisting of images of houses set in their natural surroundings, and nonface objects. Our primary goal was to compare the effects of face inversion to the effects of scene inversion in order to gain new insight into the neural origins of the face inversion effect. We were particularly interested in four issues. First, would face inversion lead to greater engagement of regions involved in generic object processing, as suggested by earlier studies? Second, to what extent would scene inversion lead to a behavioral penalty, and would that penalty be reflected in a similar shift towards greater engagement of generic object-processing regions? Third, are changes in the fMRI response engendered by face and scene inversion closely tied to the corresponding behavioral effects? Fourth, would inversion of scenes and faces have effects on regions outside of the occipitotemporal visual areas that were the focus of earlier studies? To anticipate, we found that face inversion does lead to greater engagement of generic object processing regions, scene inversion has a qualitatively similar though less dramatic effect, the magnitude of these neural effects are not tightly coupled to the magnitude of the behavioral inversion effects, and both face and scene inversion have large effects on many cortical regions that may be involved in post-recognition processing.

Section snippets

Subjects

Twelve healthy right-handed volunteers (six males, median age 20.5 years) were recruited from the local community and gave informed consent according to procedures approved by the University of Pennsylvania institutional review board. All subjects had normal or corrected-to-normal vision.

fMRI parameters

Subjects were scanned at the Hospital of the University of Pennsylvania on a 3 T Siemens Trio scanner equipped with a Siemens body coil and a four-channel head coil. T2* weighted images sensitive to blood

Behavioral results

Reaction times to correct trials were examined (Table 1). An omnibus analysis of variance revealed significant main effects of stimulus type [F(2,22) = 12.4, p < 0.001] stimulus orientation [F(1,11) = 40.6, p < 0.001] and run [F(3,33) = 18.8, p < 0.001]. Critically, we also observed a significant stimulus type × stimulus orientation interaction [F(2,22) = 4.8, p < 0.02], reflecting the fact that increases in reaction time after both face and scene inversion were significantly greater than the increases in RT

Discussion

We examined the behavioral and neural consequences of face and scene inversion with the aim of identifying similarities and differences between the effects induced by these two manipulations. In particular, we addressed four questions. First, does face inversion lead to greater engagement of regions involved in generic object processing? Second, does scene inversion lead to a behavioral penalty and a similar shift towards greater engagement of generic object-processing regions? Third, can we

Acknowledgements

We thank Elaina Lord, Justin Lacasse, Nick Tang, Paul Hirshorn, and Mark Brack for their assistance with this experiment, and Paul Downing and Martha Farah for comments on the manuscript. This research was supported in part by NIMH/NINDS grant NS045839 to the Center for Functional Neuroimaging at the University of Pennsylvania and funds provided by the School of Arts and Sciences.

References (73)

  • K. Grill-Spector et al.

    The lateral occipital complex and its role in object recognition

    Vision Research

    (2001)
  • T. Hartley et al.

    The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans

    Neuron

    (2003)
  • U. Hasson et al.

    Large-scale mirror-symmetry organization of human occipito-temporal object areas

    Neuron

    (2003)
  • J.V. Haxby et al.

    The effect of face inversion on activity in human neural systems for face and object perception

    Neuron

    (1999)
  • T. Ino et al.

    Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus

    Neuroscience Letters

    (2002)
  • N. Kanwisher et al.

    The effect of face inversion on the human fusiform face area

    Cognition

    (1998)
  • S. Kastner et al.

    Increased activity in human visual cortex during directed attention in the absence of visual stimulation

    Neuron

    (1999)
  • D.T. Leube et al.

    Brain regions sensitive to the face inversion effect: A functional magnetic resonance imaging study in humans

    Neuroscience Letters

    (2003)
  • R. Malach et al.

    The topography of high-order human object areas

    Trends in Cognitive Sciences

    (2002)
  • D. Maurer et al.

    The many faces of configural processing

    Trends in Cognitive Sciences

    (2002)
  • M.F. Mendez et al.

    Agnosia for scenes in topographagnosia

    Neuropsychologia

    (2003)
  • K.N. Ochsner

    Current directions in social cognitive neuroscience

    Current Opinion in Neurobiology

    (2004)
  • J. O’Doherty et al.

    Beauty in a smile: The role of medial orbitofrontal cortex in facial attractiveness

    Neuropsychologia

    (2003)
  • G. Rhodes et al.

    What's lost in inverted faces?

    Cognition

    (1993)
  • G. Yovel et al.

    Face perception: Domain specific, not process specific

    Neuron

    (2004)
  • E. Zarahn et al.

    Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions

    Neuroimage

    (1997)
  • G.K. Aguirre et al.

    Topographical disorientation: A synthesis and taxonomy

    Brain

    (1999)
  • G.K. Aguirre et al.

    Stimulus inversion and the responses of face and object-sensitive cortical areas

    Neuroreport

    (1999)
  • B.T. Backus et al.

    Human cortical activity correlates with stereoscopic depth perception

    Journal of Neurophysiology

    (2001)
  • J. Cao

    The size of the connected components of excursion sets of chi(2), t and F fields

    Advances in Applied Probability

    (1999)
  • S. Carey et al.

    From piecemeal to configurational representation of faces

    Science

    (1977)
  • D. Cox et al.

    Contextually evoked object-specific responses in human visual cortex

    Science

    (2004)
  • W.A. Cunningham et al.

    Neural components of social evaluation.

    Journal of Personality & Social Psychology

    (2003)
  • R. Diamond et al.

    Why faces are and are not special: An effect of expertise

    Journal of Experimental Psychology. General

    (1986)
  • P.E. Downing et al.

    A cortical area selective for visual processing of the human body

    Science

    (2001)
  • R.A. Epstein

    The cortical basis of visual scene processing

    Visual Cognition

    (2005)
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