Early Category-Specific Cortical Activation Revealed by Visual Stimulus Inversion

de Gelder B (2008) Early Category-Specific Cortical Activation Revealed by Visual Stimulus Inversion. PLoS ONE 3(10): e3503. doi:10.1371/journal.pone.0003503 Early Category-Specific Cortical Activation Revealed by Visual Stimulus Inversion Hanneke K. M. Meeren 0 Nouchine Hadjikhani 0 Seppo P. Ahlfors 0 Matti S. Ha ma la inen 0 Beatrice 0 Ernest Greene, University of Southern California, United States of America 0 1 Cognitive and Affective Neuroscience Laboratory, Tilburg University , Tilburg , The Netherlands , 2 MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts, United States of America, 3 Harvard-MIT Health Sciences and Technology , Cambridge, Massachusetts , United States of America, 4 Brain Mind Institute, EPFL , Lausanne , Switzerland Visual categorization may already start within the first 100-ms after stimulus onset, in contrast with the long-held view that during this early stage all complex stimuli are processed equally and that category-specific cortical activation occurs only at later stages. The neural basis of this proposed early stage of high-level analysis is however poorly understood. To address this question we used magnetoencephalography and anatomically-constrained distributed source modeling to monitor brain activity with millisecond-resolution while subjects performed an orientation task on the upright and upside-down presented images of three different stimulus categories: faces, houses and bodies. Significant inversion effects were found for all three stimulus categories between 70-100-ms after picture onset with a highly category-specific cortical distribution. Differential responses between upright and inverted faces were found in well-established face-selective areas of the inferior occipital cortex and right fusiform gyrus. In addition, early category-specific inversion effects were found well beyond visual areas. Our results provide the first direct evidence that category-specific processing in high-level category-sensitive cortical areas already takes place within the first 100-ms of visual processing, significantly earlier than previously thought, and suggests the existence of fast category-specific neocortical routes in the human brain. - Funding: This research was funded by the National Institutes of Health (NIH grant no. RO1NS44824 to NH) and the Netherlands Organization for Scientific Research (NWO grants no. R 95-403 and no. 451-05-014 to HKMM). MSH, SPA and BdG were supported by the MIND institute, MSH by the Center for Functional Neuroimaging Technologies (NIH grant P41 RR14075), SPA by The Whitaker Foundation (RG-01-0294) and NH by the Swiss National Foundation (PPOOB 110741). Partial support was also provided by the HFSP grant RGP0054/2004-C to BdG. Competing Interests: The authors have declared that no competing interests exist. We have the remarkable ability to recognize thousands of visual objects in our daily environment, such as faces, bodies, cars, keys, shoes, animals, food, tools, and houses. Despite its complexity, visual categorization is executed rapidly and effortlessly by the human brain. These computations appear to be mainly carried out by the ventral visual pathway [1,2], through neurons with increasingly larger receptive fields, responding to increasingly complex features of the stimuli as one moves up within the hierarchy. The physical features of the input image are generally assumed to be first extracted in lower-level cortical areas (i.e., V1, V2, V4) [3,4] before they are projected to higher-level regions in the occipito-temporal cortex where complex patterns are processed [58] and a visual representation of the input image is formed [9]. Functional neuroimaging studies (e.g. positron emission tomography, functional magnetic resonance imaging (fMRI)) in humans have examined the higher-level cortical regions involved in the visual perception of different objects. Faces [1014], bodies [15 17], animals [18,19], houses [2022], tools [18,19] and letter strings [2325] have been shown to selectively activate focal regions of cortex. While the location of areas involved in object processing has been widely studied, the sequence and timing of activation of these areas is less well known. The long-held general assumption is that at least during the first 100-ms complex visual stimuli are generally processed in the same low-level areas [26], and that category-specific cortical activation occurs at later stages. For instance, intracranial recordings in patients have shown that during face perception the well-established face-selective area of the fusiform gyrus becomes strongly activated around 170-ms after stimulus onset [24,2628]. This time course is corroborated by a prominent face-selective component around 170-ms [29] in recordings of electrical (EEG) and magnetic (MEG) brain activity from the scalp in healthy volunteers, labeled the N170 [30] in EEG studies or M170 in MEG recordings. However, this traditional model of object perception is challenged by recent psychophysical and electrophysiological findings suggesting that visual categorization processes may already take place at even earlier latencies [3135], i.e. around 100-ms post stimulus onset. Thorpe and colleagues [32,35] found evidence for rapid visual categorization (the detection of animals versus non-animals in natural images) taking place within the first 100150-ms after stimulus onset. In addition, category-specificity has also been claimed for an earlier component that peaks around 100120-ms after the onset of a visual stimulus in posterior sensors in EEG or MEG recordings, labeled the P1 and M100 component respectively, or of even earlier activity (30110-ms post-stimulus). Most of these interpretations are however heavily debated, as they were either based on inter-categorical comparisons [3639] which suffer from serious low-level confounds [40], or on old-novel distinctions which may signal general repetition effects rather than face-recognition per se [4144]. More convincing evidence for rapid face categorization was nevertheless provided by two studies free from low-level stimulus confounds. Liu and colleagues [33] found that the M100 component is sensitive to the successful detection of faces embedded in noise. In addition, Debruille et al. found early differential responses between carefully matched photographs of known and unknown faces around 100-ms at frontocentral and centroparietal sites [45]. The neuronal underpinnings of this proposed early phase of visual categorization analysis remain however a puzzle. Reports on the neuronal origin of the P1/M100 response to faces have been inconsistent, as sources have been found in the retinotopic cortex of the medial occipital cortex [36,46], posterior extrastriate cortex [47,48], but also in high-level visual cortex of the mid-fusiform gyrus [47]. We took advantage of the high temporal resolution of magnetoencephalography (MEG) combined with (...truncated)