David Pitcher

TMS Evidence for the Involvement of the Right Occipital Face Area in Early Face Processing

Extensive research has demonstrated that several specialized cortical regions respond preferentially to faces. One such region, located in the inferior occipital gyrus, has been dubbed the occipital face area (OFA). The OFA is the first stage in two influential face-processing models, both of which suggest that it constructs an initial representation of a face, but how and when it does so remains unclear. The present study revealed that repetitive transcranial magnetic stimulation (rTMS) targeted at the right OFA (rOFA) disrupted accurate discrimination of face parts but had no effect on the discrimination of spacing between these parts. rTMS to left OFA had no effect. A matched part and spacing discrimination task that used house stimuli showed no impairment. In a second experiment, rTMS to rOFA replicated the face-part impairment but did not produce the same effect in an adjacent area, the lateral occipital cortex. A third experiment delivered double pulses of TMS separated by 40 ms at six periods after stimulus presentation during face-part discrimination. Accuracy dropped when pulses were delivered at 60 and 100 ms only. These findings indicate that the rOFA processes face-part information at an early stage in the face-processing stream.

Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex

Neuroscientists have long debated whether focal brain regions perform specific cognitive functions [1-5], and the issue remains central to a current debate about visual object recognition. The distributed view of cortical function suggests that object discrimination depends on dispersed but functionally overlapping representations spread across visual cortex [6-8]. The modular view claims different categories of objects are discriminated in functionally segregated and specialized cortical areas [9-11]. To test these competing theories, we delivered transcranial magnetic stimulation (TMS) over three adjacent functionally localized areas in extrastriate cortex. In three experiments, participants performed discrimination tasks involving faces, bodies, and objects while TMS was delivered over the right occipital face area (rOFA) [12], the right extrastriate body area (rEBA) [13], or the right lateral occipital area (rLO) [14]. All three experiments showed a task selective dissociation with performance impaired only by stimulation at the site selective for that category: TMS over rOFA impaired discrimination of faces but not objects or bodies; TMS over rEBA impaired discrimination of bodies but not faces or objects; TMS over rLO impaired discrimination of objects but not faces or bodies. The results support a modular account in which category-selective areas contribute solely to discrimination of their preferred categories.

Transcranial Magnetic Stimulation Disrupts the Perception and Embodiment of Facial Expressions

Theories of embodied cognition propose that recognizing facial expressions requires visual processing followed by simulation of the somatovisceral responses associated with the perceived expression. To test this proposal, we targeted the right occipital face area (rOFA) and the face region of right somatosensory cortex (rSC) with repetitive transcranial magnetic stimulation (rTMS) while participants discriminated facial expressions. rTMS selectively impaired discrimination of facial expressions at both sites but had no effect on a matched face identity task. Site specificity within the rSC was demonstrated by targeting rTMS at the face and finger regions while participants performed the expression discrimination task. rTMS targeted at the face region impaired task performance relative to rTMS targeted at the finger region. To establish the temporal course of visual and somatosensory contributions to expression processing, double-pulse TMS was delivered at different times to rOFA and rSC during expression discrimination. Accuracy dropped when pulses were delivered at 60–100 ms at rOFA and at 100–140 and 130–170 ms at rSC. These sequential impairments at rOFA and rSC support embodied accounts of expression recognition as well as hierarchical models of face processing. The results also demonstrate that nonvisual cortical areas contribute during early stages of expression processing.

The role of the occipital face area in the cortical face perception network

Functional magnetic resonance imaging (fMRI) studies have identified spatially distinct face-selective regions in human cortex. These regions have been linked together to form the components of a cortical network specialized for face perception but the cognitive operations performed in each region are not well understood. In this paper, we review the evidence concerning one of these face-selective regions, the occipital face area (OFA), to better understand what cognitive operations it performs in the face perception network. Neuropsychological evidence and transcranial magnetic stimulation (TMS) studies demonstrate the OFA is necessary for accurate face perception. fMRI and TMS studies investigating the functional role of the OFA suggest that it preferentially represents the parts of a face, including the eyes, nose, and mouth and that it does so at an early stage of visual perception. These studies are consistent with the hypothesis that the OFA is the first stage in a hierarchical face perception network in which the OFA represents facial components prior to subsequent processing of increasingly complex facial features in higher face-selective cortical regions.

Differential selectivity for dynamic versus static information in face-selective cortical regions

Neuroimaging studies have identified multiple face-selective regions in human cortex but the functional division of labor between these regions is not yet clear. A central hypothesis, with some empirical support, is that face-selective regions in the superior temporal sulcus (STS) are particularly responsive to dynamic information in faces, whereas the fusiform face area (FFA) computes the static or invariant properties of faces. Here we directly tested this hypothesis by measuring the magnitude of response in each region to both dynamic and static stimuli. Consistent with the hypothesis, we found that the response to movies of faces was not significantly different from the response to static images of faces from these same movies in the right FFA and right occipital face area (OFA). By contrast the face-selective region in the right posterior STS (pSTS) responded nearly three times as strongly to dynamic faces as to static faces, and a face-selective region in the right anterior STS (aSTS) responded to dynamic faces only. Both of these regions also responded more strongly to moving faces than to moving bodies, indicating that they are preferentially engaged in processing dynamic information from faces, not in more general processing of any dynamic social stimuli. The response to dynamic and static faces was not significantly different in a third face-selective region in the posterior continuation of the STS (pcSTS). The strong selectivity of face-selective regions in the pSTS and aSTS, but not the FFA, OFA or pcSTS, for dynamic face information demonstrates a clear functional dissociation between different face-selective regions, and provides further clues into their function.

Two Critical and Functionally Distinct Stages of Face and Body Perception

Cortical regions that respond preferentially to particular object categories, such as faces and bodies, are essential for visual perception of these object categories. However, precisely when these regions play a causal role in recognition of their preferred categories is unclear. Here we addressed this question using transcranial magnetic stimulation (TMS). Across a series of experiments, TMS was delivered over the functionally localized right occipital face area (rOFA) or right extrastriate body area (rEBA) at different latencies, up to 150 ms, after stimulus onset while adult human participants performed delayed match-to-sample tasks on face and body stimuli. Results showed that TMS disrupted task performance during two temporally distinct time periods after stimulus onset, the first at 40/50 ms and the second at 100/110 ms. These two time periods exhibited functionally distinct patterns of impairment: TMS delivered during the early time period (at 40/50 ms) disrupted task performance for both preferred (faces at rOFA and bodies at rEBA) and nonpreferred (bodies at rOFA and faces at rEBA) categories. In contrast, TMS delivered during the later time period (at 100/110 ms) disrupted task performance for the preferred category only of each area (faces at rOFA and bodies at rEBA). These results indicate that category-selective cortical regions are critical for two functionally distinct stages of visual object recognition: an early, presumably preparatory stage that is not category selective occurring almost immediately after stimulus onset, followed by a later stage of category-specific perceptual processing.

Combined TMS and fMRI Reveal Dissociable Cortical Pathways for Dynamic and Static Face Perception

Faces contain structural information, for identifying individuals, as well as changeable information, which can convey emotion and direct attention. Neuroimaging studies reveal brain regions that exhibit preferential responses to invariant [1, 2] or changeable [3-5] facial aspects but the functional connections between these regions are unknown. We addressed this issue by causally disrupting two face-selective regions with thetaburst transcranial magnetic stimulation (TBS) and measuring the effects of this disruption in local and remote face-selective regions with functional magnetic resonance imaging (fMRI). Participants were scanned, over two sessions, while viewing dynamic or static faces and objects. During these sessions, TBS was delivered over the right occipital face area (rOFA) or right posterior superior temporal sulcus (rpSTS). Disruption of the rOFA reduced the neural response to both static and dynamic faces in the downstream face-selective region in the fusiform gyrus. In contrast, the response to dynamic and static faces was doubly dissociated in the rpSTS. Namely, disruption of the rOFA reduced the response to static but not dynamic faces, while disruption of the rpSTS itself reduced the response to dynamic but not static faces. These results suggest that dynamic and static facial aspects are processed via dissociable cortical pathways that begin in early visual cortex, a conclusion inconsistent with current models of face perception [6-9].

The role of lateral occipital face and object areas in the face inversion effect

Stimulus inversion impairs face discrimination to a greater extent than discrimination of other non-face object categories. This finding has led to suggestions that upright faces are represented by mechanisms specialized for upright faces whereas inverted face representation depends on more general object recognition mechanisms. In the present study we tested the causal role of face-selective and object-selective cortical areas for upright and inverted face discrimination by transiently disrupting neural processing using transcranial magnetic stimulation (TMS). Participants matched upright and inverted faces while TMS was delivered over each participants functionally localized right occipital face area (rOFA) or right lateral occipital area (rLO). TMS delivered over rOFA disrupted the discrimination of upright and inverted faces while TMS delivered over rLO impaired inverted face discrimination only. These results provide causal evidence that upright faces are represented by face-specific mechanisms whereas inverted faces are represented by both face-specific and object-specific mechanisms. The similar sensitivity of the OFA to upright and inverted faces is consistent with the hypothesis that the OFA processes facial features at an early stage of face processing.

Facial Expression Recognition Takes Longer in the Posterior Superior Temporal Sulcus than in the Occipital Face Area

Neuroimaging studies have identified a face-selective region in the right posterior superior temporal sulcus (rpSTS) that responds more strongly during facial expression recognition tasks than during facial identity recognition tasks, but precisely when the rpSTS begins to causally contribute to expression recognition is unclear. The present study addressed this issue using transcranial magnetic stimulation (TMS). In Experiment 1, repetitive TMS delivered over the rpSTS of human participants, at a frequency of 10 Hz for 500 ms, selectively impaired a facial expression task but had no effect on a matched facial identity task. In Experiment 2, participants performed the expression task only while double-pulse TMS (dTMS) was delivered over the rpSTS or over the right occipital face area (rOFA), a face-selective region in lateral occipital cortex, at different latencies up to 210 ms after stimulus onset. Task performance was selectively impaired when dTMS was delivered over the rpSTS at 60–100 ms and 100–140 ms. dTMS delivered over the rOFA impaired task performance at 60–100 ms only. These results demonstrate that the rpSTS causally contributes to expression recognition and that it does so over a longer time-scale than the rOFA. This difference in the length of the TMS induced impairment between the rpSTS and the rOFA suggests that the neural computations that contribute to facial expression recognition in each region are functionally distinct.

Stimulation of category-selective brain areas modulates ERP to their preferred categories.

Neural selectivity to specific object categories has been demonstrated in extrastriate cortex with both functional MRI [1-3] and event-related potential (ERP) [4, 5]. Here we tested for a causal relationship between the activation of category-selective areas and ERP to their preferred categories. Electroencephalogram (EEG) was recorded while participants observed faces and headless bodies. Concurrently with EEG recording, we delivered two pulses of transcranial magnetic stimulation (TMS) over the right occipital face area (OFA) or extrastriate body area (EBA) at 60 and 100 ms after stimulus onset. Results showed a clear dissociation between the stimulated site and the stimulus category on ERP modulation: stimulation of the OFA significantly increased the N1 amplitude to faces but not to bodies, whereas stimulation of the EBA significantly increased the N1 amplitude to bodies but not to faces. These findings provide the first evidence for a specific and causal link between activity in category-selective networks and scalp-recorded ERP to their preferred categories. This result also demonstrates that the face and body N1 reflects several nonoverlapping neural sources, rather than changes in face-selective mechanisms alone. Lastly, because early stimulation (60-100 ms) affected selectivity of a later ERP component (150-200 ms), the results could imply a feed-forward connection between occipital and temporal category-selective areas.