Elsevier

NeuroImage

Volume 43, Issue 1, 15 October 2008, Pages 156-164
NeuroImage

Position-specific and position-invariant face aftereffects reflect the adaptation of different cortical areas

https://doi.org/10.1016/j.neuroimage.2008.06.042Get rights and content

Abstract

Adaptation to faces leads to face aftereffects and currently this topic attracts a lot of attention because it clearly shows that adaptation occurs even at the higher stages of visual cortical processing. Recently it has been found that long-term exposure to a face stimulus results in adaptation of a position-specific population of face sensitive neurons in addition to a position-invariant neural population, the later being also adapted in the case of short-term adaptation. Here we used the fMRI adaptation technique to investigate the neural locus of position-specific and position-invariant face adaptation. We show that in the right fusiform face area adaptation effects are position invariant and can be evoked by short (500 ms) as well as long (4500 ms) adaptation durations. On the other hand adaptation effects in the right occipital face area are position-specific and require long-term adaptation to develop. These findings imply that the behaviourally observed face aftereffects reflect time-dependent adaptation processes of both position-specific and invariant face sensitive neurons at different stages of visual processing.

Introduction

Prolonged exposure to faces leads to robust facial aftereffects (Leopold et al., 2001, Rhodes et al., 2003, Yamashita et al., 2005, Webster and MacLin, 1999, Webster et al., 2004). Unlike adaptation effects to basic, low-level visual dimensions — i.e. motion, orientation, spatial frequency or texture (for review see Anstis et al., 1988; Frisby, 1979, Durgin and Proffitt, 1996, Clifford, 2002), facial adaptation (FA) is associated with high-level brain areas, containing face-selective neurons. One argument for the high-level nature of FA would be its invariance to the physical characteristics of the stimuli. Indeed, Leopold et al. (2001) found that adaptation to face identity generalizes across retinal positions up to 6°, while Fang et al. (2006), using floating adapters in an approximately 10° by 10° area, also found viewpoint aftereffects. Hierarchically higher processing steps in FA are suggested by other evidences, such as the fact that face aftereffects are, to a large extent, also invariant to changes in size (Zhao and Chubb, 2001, Rhodes et al., 2004, Anderson and Wilson, 2005, Kovács et al., 2006), orientation (Rhodes et al., 2003, Watson and Clifford, 2003), color and contrast (Yamashita et al., 2005). These findings support the idea that face-selective neural processes at the higher stages of visual processing, tolerating the above changes of the stimuli, can adapt and might represent the neural basis of face-specific aftereffects.

Recently however, by comparing aftereffects following different durations of visual adaptation, we showed that FA is not entirely position invariant (Kovács et al., 2005, Kovács et al., 2007).

In event-related potential (ERP) recording experiments we showed that long-term adaptation to face gender (Kovács et al., 2006) or face detection in a gaze discrimination task (Schweinberger et al., 2007) has a strong effect on the N170 component of the ERP response, which reflects the structural coding of face stimuli (Bentin et al., 1996, Rossion et al., 1999, Rossion et al., 2000b, Itier and Taylor, 2004a) and is thought to be generated in the middle and posterior part of the fusiform gyrus, in the inferior occipital cortex and also in the superior temporal gyrus (Bentin et al., 1996, Deffke et al., 2007, Halgren et al., 1999, Horovitz et al., 2004, Itier and Taylor, 2004b, Rossion et al., 2000a, Rossion et al., 2000b, Rossion et al., 2003, Schweinberger et al., 2002, Sergent et al., 1992).

Moreover, we found, that after long-term (5000 ms) adaptation the gender-specific aftereffects and the related N170 amplitude reductions are larger when the adaptor and target faces are presented on the same retinal position as compared to when they are displayed in different hemifields, while no such difference was observed after short-term (500 ms) adaptation (Kovács et al., 2005, Kovács et al., 2007). These results suggest that both short and long exposure to faces leads to adaptation of position-invariant face-selective processes, whereas adaptation of position-specific neural mechanisms of face processing requires long-term adaptation.

However, due to their limited spatial resolution, ERP recordings are not able to reveal the exact source of the N170 component, and thus cannot provide precise information about the location of the adapted neurons either. Consequently in our present fMRI adaptation experiments (fMRIa; Grill-Spector et al., 1999, Andrews and Ewbank, 2004, Grill-Spector et al., 2006, Krekelberg et al., 2006) we induced position-specific and position-invariant adaptations to peripherally presented faces. Previous fMRIa experiments have shown that the early, retinotopically organized cortical areas exhibit adaptation only after long-term exposure to the adapting stimulus (Fang et al., 2005). In contrast, in more downstream visual areas not only long-term, but already very short adaptation is able to evoke strong fMRIa effects (Henson, 2003). Thus, since previous fMRIa data as well as our own ERP results suggest that different neural populations along the visual hierarchy might differ in their dynamics of adaptation, in the present experiments we also manipulated the duration of adaptation.

Section snippets

Materials and methods

The stimuli and the task were similar to those used and described in details in recent studies by Kovács et al., 2005, Kovács et al., 2007 thus here just a brief description of these and additional details are given.

Behavioral results

The behavioural results in the scanner confirmed our previous findings that FA after long-term adaptation consists of a position-specific and position-invariant component while after short adaptation duration adaptation is completely position invariant (Kovács et al., 2005, Kovács et al., 2007). After being adapted to a female face for several seconds in the LONG condition the target faces were perceived as more masculine as compared to the Control (Fig. 2; main effect of adaptation condition: F

Discussion

The main finding of the present study is that in the occipital face area facial adaptation leads to significant reduction of fMRI responses in a position-specific manner, while adaptation effects in the fusiform face area are position invariant. Our results also show that in the FFA both long and short-term adaptation decreases the BOLD signal, whereas in the OFA only long-term adaptation results in adaptation effects.

Acknowledgments

This work was supported by a grant from the European Union (EU IST Cognitive Systems, project 027198 “Decisions in Motion”), from the Hungarian Scientific Research Fund to G.K (T049467) and by the Bolyai Fellowship to Z.V. We thank Markus Raabe and Marcin Posel for their help in the preparation of the experiments and the two anonymous reviewers for helping us improve our manuscript.

References (82)

  • Grill-SpectorK. et al.

    Differential processing of objects under various viewing conditions in the human lateral occipital complex

    Neuron

    (1999)
  • Grill-SpectorK. et al.

    The lateral occipital complex and its role in object recognition

    Vis. Res.

    (2001)
  • Grill-SpectorK. et al.

    Repetition and the brain: neural models of stimulus-specific effects

    Trends Cogn. Sci.

    (2006)
  • HassonU. et al.

    Eccentricity bias as an organizing principle for human high-order object areas

    Neuron

    (2002)
  • HaxbyJ.V. et al.

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

    Neuron

    (1999)
  • HaxbyJ.V. et al.

    Human neural systems for face recognition and social communication

    Biol. Psychiatry

    (2002)
  • HensonR.N.

    Neuroimaging studies of priming

    Progr. Neurobiology

    (2003)
  • HorovitzS.G. et al.

    Parametric design and correlational analyses help integrating fMRI and electrophysiological data during face processing

    Neuroimage

    (2004)
  • KovácsG. et al.

    Adaptation duration affects the spatial selectivity of facial aftereffects

    Vision Res.

    (2007)
  • KrekelbergB. et al.

    Adaptation: from single cells to BOLD signals

    Trends Neurosci.

    (2006)
  • MalachR. et al.

    The topography of high-order human object areas

    Trends Cogn. Sci.

    (2002)
  • MaldjianJ.A. et al.

    An automated method for neuroanatomic and cytoarchitectonic atlasbased interrogation of fMRI data sets

    Neuroimage

    (2003)
  • MenghiniF. et al.

    Neurocomputing

    (2007)
  • NasanenR.

    Spatial frequency bandwidth used in the recognition of facial images

    Vis. Res.

    (1999)
  • PitcherD. et al.

    TMS evidence for the involvement of the right occipital face area in early face processing

    Curr. Biol.

    (2007)
  • RhodesG. et al.

    Orientation-contingent face aftereffects and implications for face-coding mechanisms

    Curr. Biol.

    (2004)
  • RhodesG. et al.

    The timecourse of higher-level face aftereffects

    Vision Res.

    (2007)
  • RossionB. et al.

    Spatio-temporal localization of the face inversion effect: an eventrelated potentials study

    Biol. Psychol.

    (1999)
  • RossionB.

    Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia

    Neuroimage

    (2008)
  • RousseletG.A. et al.

    How parallel is visual processing in the ventral pathway?

    Trends Cog. Sci.

    (2004)
  • SchiltzC. et al.

    Faces are represented holistically in the human occipito-temporal cortex

    Neuroimage

    (2006)
  • SchweinbergerS.R. et al.

    Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions

    Brain Res Cogn. Brain Res.

    (2002)
  • SchweinbergerS.R. et al.

    Interhemispheric cooperation for face recognition but not for affective facial expressions

    Neuropsychologia

    (2003)
  • SorgerB. et al.

    Understanding the functional neuroanatomy of acquired prosopagnosia

    Neuroimage

    (2007)
  • Van EssenD.C.

    Windows on the brain. The emerging role of atlases and databases in neuroscience

    Curr. Op. Neurobiol.

    (2002)
  • ZhaoL. et al.

    The size-tuning of the face-distortion aftereffect

    Vis. Res.

    (2001)
  • BentinS. et al.

    Electrophysiological studies of face perception in humans

    J. Cogn. Neurosci.

    (1996)
  • BourneV.J. et al.

    Lateralized repetition priming for familiar faces: evidence for asymmetric interhemispheric cooperation

    Q. J. Exp. Psychol.

    (2006)
  • BrettM. et al.

    The problem of functional localization in the human brain

    Nat. Rev. Neurosci.

    (2002)
  • CalderA.J. et al.

    Understanding the recognition of facial identity and facial expression

    Nat. Rev. Neurosci.

    (2005)
  • DiCarloJ.J. et al.

    Anterior inferior temporal neurons of monkeys engaged in object recognition can be highly sensitive to object retinal position

    J. Neurophysiol.

    (2003)
  • Cited by (66)

    • Changes in face category induce stronger duration distortion in the temporal oddball paradigm

      2022, Vision Research
      Citation Excerpt :

      This is in line with the fact that adaptation effects are also observed for face stimuli (Fang, Ijichi, & Yantis, 2007; Oruç & Barton, 2011; Webster et al., 2004). Given that higher visual areas are responsible for face adaptation (Fang, Murray, & He, 2007; Kovács et al., 2008), our findings further suggest that high-level visual adaptation contributes to the repetition effect. In conclusion, the present study demonstrated that changes in face category from preceding stimuli can increase the duration distortion in the oddball effect, and this effect cannot be fully explained by the difference in low-level visual properties of face images used.

    • Neural adaptation in pSTS correlates with perceptual aftereffects to biological motion and with autistic traits

      2016, NeuroImage
      Citation Excerpt :

      This conclusion is consistent with recent findings from a study of face adaptation (Kaiser et al., 2013), which also found evidence for a dissociation in these two types of adaptation. The extent to which these different mechanisms are engaged likely depends on the duration of the adaptation stimulus (Fang et al., 2007b; Kovács et al., 2008; Kaiser et al., 2013). Further studies will be required to fully characterize differences in the physiological mechanisms responsible for repetition suppression effects versus perceptual adaptation aftereffects in the human brain.

    • Investigating the Causal Role of rOFA in Holistic Detection of Mooney Faces and Objects: An fMRI-guided TMS Study

      2016, Brain Stimulation
      Citation Excerpt :

      The key point is that many of such features are not tied to a specific category but rather could be indicators of objects of various stimulus types, such as a face, a guitar or an apple. Our results are consistent with previous work implicating rOFA in holistic processing of faces [52–54]. For example, Jonas and colleagues [52] showed that electrical stimulation of rOFA impaired the perception of the face as a whole.

    View all citing articles on Scopus
    View full text