Common cortical responses evoked by appearance, disappearance and change of the human face

BMC Neuroscience BioMed Central Research article Open Access Common cortical responses evoked by appearance, disappearance and change of the human face Emi Tanaka*1, Koji Inui1,2, Tetsuo Kida1 and Ryusuke Kakigi1,2,3 Address: 1Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan, 2Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan and 3RISTEX, Japan Science and Technology Agency, Tokyo, Japan E-mail: Emi Tanaka* - ; Koji Inui - ; Tetsuo Kida - ; Ryusuke Kakigi - *Corresponding author Published: 24 April 2009 BMC Neuroscience 2009, 10:38 Received: 12 September 2008 doi: 10.1186/1471-2202-10-38 Accepted: 24 April 2009 This article is available from: http://www.biomedcentral.com/1471-2202/10/38 © 2009 Tanaka et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: To segregate luminance-related, face-related and non-specific components involved in spatio-temporal dynamics of cortical activations to a face stimulus, we recorded cortical responses to face appearance (Onset), disappearance (Offset), and change (Change) using magnetoencephalography. Results: Activity in and around the primary visual cortex (V1/V2) showed luminance-dependent behavior. Any of the three events evoked activity in the middle occipital gyrus (MOG) at 150 ms and temporo-parietal junction (TPJ) at 250 ms after the onset of each event. Onset and Change activated the fusiform gyrus (FG), while Offset did not. This FG activation showed a triphasic waveform, consistent with results of intracranial recordings in humans. Conclusion: Analysis employed in this study successfully segregated four different elements involved in the spatio-temporal dynamics of cortical activations in response to a face stimulus. The results show the responses of MOG and TPJ to be associated with non-specific processes, such as the detection of abrupt changes or exogenous attention. Activity in FG corresponds to a facespecific response recorded by intracranial studies, and that in V1/V2 is related to a change in luminance. Background It has been proposed that there are specific neural processes underlying face perception. Functional magnetic resonance imaging (fMRI) and positron-emission tomography (PET) studies have shown that regions of the ventral occipito-temporal pathway of the brain, such as part of the fusiform gyrus (FG), called the fusiform face area (FFA), respond more to faces than other stimuli [1-8]. Intracranial electrophysiological recordings from the surface of the cortex have demonstrated a facespecific negative component maximum around 200 ms, N200, which was generated in the lateral part of the FG and at the border of the middle temporal gyrus and middle occipital gyrus in human patients [9-13]. Magnetoencephalography (MEG) studies have reported M100 evoked during 80–150 ms [14-16] and M200 or M170 evoked during 140–200 ms [14-22], which respond maximally to face stimuli. Numerous eventrelated potential (ERP) studies have also reported a negative component peaking 150–170 ms post-stimulus over temporo-parietal regions of the human scalp which responds maximally to face stimuli (N170) [23-28]. An earlier P1 evoked at 100–120 ms was also reported to reflect face processing [25]. Page 1 of 9 (page number not for citation purposes) BMC Neuroscience 2009, 10:38 These face-evoked EEG and MEG responses with different response latencies imply the existence of different neural sub-processes underlying face perception. Because electric and magnetic fields recorded from the scalp surface or sensors near the scalp are summations of cortical activities (this statement is less true of MEG than it is of EEG), cortical responses evoked by a face stimulus should contain not only face-specific components [2,10], but also components related to basic visual features such as changes in luminance or non-specific responses such as those related to the detection of change accompanied by passive shifts of attention [29]. For instance, responses evoked by a stimulus are destined to be associated with processes such as an orienting response or passive attention because of the intrinsic property of the methodologies. In fact, classical studies of evoked responses have long discussed the relationship between evoked responses and specific theories derived from the orienting response theory [30,31]. Also, in many natural scenes, responses evoked by seeing a face would involve neural activity sensitive to luminance. Previous face studies have compared responses to faces, other objects and scrambled faces, or manipulated a variety of factors affecting face recognition to examine face selectivity or other importance issues on face recognition [14,15,20,22,25,26,32]. In addition, a large number of studies have revealed the generators of facerelated responses [16,21,28,32-34]. However, these paradigms cannot reveal which subcomponents wholehead activity for a face includes. For example, most previous studies examining face selectivity have also taken a subcomponent such as luminance-related activity into account by comparing cortical response to faces with other objects with the same luminance, but have not attempted to extract luminance-related subprocesses from the recorded activity. In this study, we attempted to segregate different components, luminance-related, face-related and non-specific, involved in the recorded activity in response to a face stimulus. To this end, we used whole-head MEG to record cortical responses evoked by each of three kinds of face stimuli; appearance of a face (Onset), disappearance of the face (Offset), and change from one face to another (Change) against a uniform background. The results of comparisons among these responses were hypothesized as follows. (1) Responses in brain areas involved in face recognition will not appear for Offset. (2) Responses in areas involved in changes in mean luminance will be smaller for Change than for the other two stimuli, because Change occurred without a change in mean luminance. (3) Finally, responses in areas involved in non-specific processes such as the detection of abrupt changes will appear commonly to all stimuli. The http://www.biomedcentral.com/1471-2202/10/38 segregation of cortical responses related to basic visual, face-related and non-specific features from the recorded activity, would promote the understanding of facerelated neural processing. Methods Subjects Recordings were obtained from 14 healthy right-handed subjects (seven males, seven females), aged 25–55 years old (mean 35.4 ± 10.4). The present study was approved in advance (...truncated)