Electrophysiological Studies of Human Face Perception. III: Effects of Top-down Processing on Face-specific Potentials

“ERP studies using long-lag repetition of faces, including studies that record directly from the cortical surface (in patients undergoing surgery [ 53 ]), tend to find that repetition effects emerge only after the first face-specific ERP component, the ‘N170’ [54,55].”

“…1985; Puce et al., 1999) and repetitive transcranial stimulation (Stewart , Meyer, Frith, & Rothwell, 2001) of similar regions interferes with recognition processes or, in some cases, can create an illusory percept of an object or a face (Puce et al., 1999; Lee, Hong, Seo, Tae, & Hong, 2000).”

“A powerful demonstration of the causal role of these regions in face perception comes from two studies demonstrating that electrical stimulation of these ventral temporal sites can produce a transient inability to identify faces (Puce et al. 1999; Mundel et al. 2003).”

“Evoked potential studies using electrodes placed on the cortical surface in patients undergoing brain surgery for temporal lobe epilepsy have shown that sites in these same cortical regions produce facespecific responses (Allison et al 1999; McCarthy et al 1999; Puce et al 1999).”

“…is supported by electrophysiological data: Field potentials in human temporal visual cortex are modulated by emotional or social information (Puce et al., 1999), and single neurons in monkey temporal cortex encode information about the emotion shown in the face at a point in time later than…”

“There may be columns of neurons specialized for the recognition of letters, graphemes, or words, but they are likely to be intermixed with other neurons involved in object and face recognition (Puce et al., 1999).”

“face-specific) potentials, onsetting 150–200 ms post-stimulus, but little evidence that these potentials are sensitive to prior experience with the objects; such effects only emerge 250–300 ms post-stimulus (Puce et al., 1999).”

“N170 and the lateral N200 could reflect similar processes, despite the difference in timing.”

“First, Kanwisher (this issue) suggests that face selectivity in the FFA as revealed by functional magnetic resonance imaging (fMRI) reflects a special-purpose, innate mechanism for detecting the geometry of faces, that is, a mechanism that determines only that a face is a face, but not the individual identity of the f…”

“In pharmaco-resistant epileptic patients implanted with sub-dural electrodes for surgery, the N200, a negative wave directly recorded on the cortical surface, is selective to faces but also to face parts such as the eye region (Allison et al., 1994a,b, 1999; McCarthy et al., 1999; Puce et al., 1999).”

“, and electrical stimulation in these regions interferes with recognitio”

“, 1994), stimulation studies (Puce et al., 1999; Mundel et al., 2003) and neuropsychological studies (Wada and Yamamoto, 2001), our finding that some regions in the ventral visual pathway are apparently strongly selective for a single class of visual stimuli would seem to argue against the idea that all regions in the…”

“…patterns of activations (Martin et al., 1996; Kanwisher et al., 1997; Aguirre et al., 1998; Cappa et al., 1998; Epstein and Kanwisher, 1998; Chao et al., 1999; Haxby et al., 1999; Ishai et al., 1999; Puce et al., 1999; Thompson-Schill et al., 1999; Downing et al., 2001; Devlin et al., 2002).”

“…of the human temporal lobe in patients undergoing resection surgery and found that a late event related potential (ERP) termed the P350 localized to the inferior ATL was preferentially sensitive to faces and face priming (Allison et al., 1999; Puce et al., 1999); see also Barbeau et al. (2008).”

“(C) Magnitude of intracranial ERP components to face repetitions, expressed relative to first presentation, with example electrode sites from one patient inset (reprinted with permission of Oxford University Press from Puce et al. [ 28 ]).”

“For the first time, Retzius describes the Sulcus sagittalis gyri fusiformis with nearly the exact definition used by modern authors (Nasr et al., 2011; Nobre et al., 1998; Puce et al., 1996; Puce et al., 1999; Weiner et al., 2014; Weiner and GrillSpector, 2010, 2013; Weiner et al., 2010).”

“Their activity is reduced when facial features components in ventral occipital and temporal areas are rearranged, or only single face component are pre- [1,22,28].”

“In conclusion, the present scalp-recorded N170 data converge with the previously published pattern of the intracranially recorded N200 data (for a comprehensive review see Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999), supporting a multifunctional organization of the structural encoding mechanism for…”

“…at 100 ms would then precede the timing of the intracranial ERP responses to faces recorded in the right fusiform gyrus of neuropsychological patients that has been shown peak at times varying from 110 to 700 ms (Allison et al. 1999; McCarthy et al. 1999; Puce et al. 1999; Barbeau et al. 2008).”

“A gradual temporal evolution of these interactions may explain why the later, but not initial, facespecific fusiform cortical ERPs are modulated by recognition (Puce et al., 1999).”

“…a cluster of brain regions in the ventral visual stream known as the lateral occipital complex (LOC; e.g. Kohler et al., 1995; Malach et al., 1995; Puce et al., 1996, 1999; Kanwisher et al., 1997; Allison et al., 1999; Haxby et al., 1999; Ishai et al., 1999; Doniger et al., 2000, 2001, 2002;…”

“Face-selective potentials were found in several sites along ventral occipitotemporal and lateral temporal cortices (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999), as well as the amygdala and prefrontal structures (Halgren et al., 1994a,b; Barbeau et al., in press).”

“These findings have led to the interpretation that the ventral temporal cortex contains anatomically segregated modules that are category-specific ( Puce et al., 1999; Aguirre et al., 1998; Kanwisher et al., 1997; Allison et al., 1994).”

“repeated objects, observed here using fMRI, may also be similar to reductions in intracranial event-related potentials, recently reported by Puce, Allison, and McCarthy [43] for repeatedly presented faces.”

“While the latency of this negative peak in this subject is faster than several prior publications (Allison et al., 1994; Puce et al., 1999) it is likely the same ERP, as there are interindividual differences in response latencies.”

“…and temporally resolved investigation of the face perception system (Allison et al., 1994a,b, 1999; Halgren et al., 1994a,b; McCarthy et al., 1999; Puce et al., 1999); but their scope was limited to the electrical potentials evoked by (i.e., phase-locked to) visual stimuli or to a limited view of…”

“…found activation in the STS and the amygdala , regions that mediate the processing of information relevant to social communication, for example, eye gaze direction (Puce et al., 1999; Hoffman and Haxby, 2000) and facial expression (Breiter et al., 1996; Morris et al., 1996; Phillips et al., 1997).”

“…are plotted for three important face-processing areas: the fusiform face area (FFA) in black; the occipital face area (OFA) in red; and the superior temporal sulcus (STS) in purple (Haxby et al., 1994; Kanwisher et al., 1997; Halgren et al., 1999; Puce et al., 1999; Rossion et al., 2003a,b).”

“ERP studies in humans (Bentin et al., 1999; Eimer, 2000; Puce et al., 1999) have shown that the initial response to faces, the N170 potential, is not modulated by familiarity or stimulus repetition, but later responses to faces (between 200 and 500 ms) are sensitive to familiarity (these later responses are located ov…”

“Allison et al. (1994, 1999), McCarthy, Puce, Belger, and Allison (1999), and Puce, Allison, and McCarthy (1999) reported a negative component to faces, at about 200 msec (N200), at various sites on the fusiform and inferior temporal gyri that suggested the presence of discrete, specialized regions for processing faces.”

“ERP studies have attributed a source of face selectivity (face-specific AP350s) to the anterior ventral temporal pole (6), and this ERP component has been sensitive for priming and habituation paradigms involving faces (27).”

“…of recent evidence gathered from intracranial ERP recordings suggesting that there may be two separate sources of face-sensitive activity approximately 200 ms poststimulus, one in the FG and one in the lateral occipitotemporal cortex (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“specific’ component) can be modulated by familiarity (Puce et al., 1999), raising the possibility that familiarity-related fusiform”

“…[Cox et al., 2004; Peelen and Downing, 2005], and that cortical regions adjacent to the FFA are selective for body parts [McCarthy et al., 1999; Peelen and Downing, 2005; Puce et al., 1999], and the response of these regions often gets averaged in with the FFA when scanning at standard resolution.”

“…(Sergent et al. 1992, Sergent & Signoret 1992), then with intracranial electroencephalography (Allison et al. 1994a,b, 1999; McCarthy et al. 1999; Puce et al. 1999), and later with functional magnetic resonance imaging (fMRI) (Kanwisher et al. 1997, McCarthy et al. 1997, Pinsk et al. 2009, Puce…”

“As described above for the Rees et al. (1999) study, simply focusing visual attention on different aspects of an unchanging stimulus has a strong effect on the content and intensity of perceptual awareness.”

“Intracranial electrophysiological studies in humans have reported face-selective FG responses (Allison et al., 1994a,b; Puce et al., 1999; Murphey et al., 2009; Parvizi et al., 2012) that are sensitive to stimulus properties (Davidesco et al.”

“The onset latency of the present long-lag ERP repetition effect (from 200 to 300 ms) is earlier than is typically found using word or faces (Henson and Rugg, 2002; Puce et al., 1999).”

“Indeed, intracranial recordings of face specific N200 responses from the fusiform gyrus have shown that full faces evoke larger N200 than do isolated eyes [McCarthy et al., 1999], but the N200 response amplitude in face-specific sites decreases progressively in the order of faces, eyes, contours, lips, and noses, sugg…”

“D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:7, pp. 1150–1167 tion of face-specific ERP sites located in the fusiform gyrus most commonly results in a transient failure to identify, rather than detect, faces (Mundel et al., 2003; Puce, Allison, & McCarthy, 1999 ).”

“Intracranial recordings comparing the response to images of hands and faces (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999 ) have provided three findings that bear on the present results: (1) face-selective recordings were made from the lateral and ventral occipitotemporal surface; (2) hand-selective…”

“Interestingly, on the basis of intracranial event-related potential (ERP) studies, Puce et al. (1999) reported that face-speci®c sites were typically anterior to letter-speci®c sites in the occipitotemporal cortex.”

“…FFA and STG/STS have been implicated previously in early visual processing of faces using neuroimaging (Puce et al., 1995, 1998; Kanwisher et al., 1997; Haxby et al., 2000; Hoffman and Haxby, 2000) and field potential recordings on the cortical surface (Allison et al., 1999; Puce et al., 1999b,a).”

“, 1999), following an earlier face-specific N200 originating from posterior ventral temporal cortex (Puce et al., 1999).”

“Intracranial recordings are also consistent with this view (Puce et al., 1999).”

“Intracranial recordings also suggest that there may be multiple generators of the N170/N200 component in the FG and superior temporal sulcus (STS, Puce et al., 1999).”

“The classic studies by Allison, Ginter, et al. (1994), Allison, McCarthy, et al. (1994), Allison et al. (1999), McCarthy et al. (1999), and Puce et al. (1999) using grids on the cortical surface identified a series of components evoked by faces.”

“Electrical stimulation of these regions corroborates these results by demonstrating temporary inability to name familiar faces or by evoking face-related hallucinations (Allison et al. 1994, Puce et al. 1999).”

“However, whether the results so far suggest that both face familiarity (Campanella et al., 2000) and face expression affect structural encoding if the task requires face matching, we have to note that some studies showed that face familiarity has no effect neither on intracranial N200 ( Puce, Allison, & McCarthy, 1999…”

“Studies using functional magnetic resonance imaging (fMRI) (Kanwisher, McDermott, & Chun, 1997; McCarthy, Puce, Gore, & Allison, 1997), event-related potentials (Eimer, 2000; McCarthy, Puce, Belger, & Allison, 1999; Puce, Allison, & McCarthy, 1999; Bentin, Allison, Puce, Perez, & McCarthy, 1996), and single-cell recor…”

“The ventral stream has been implicated in the processing of facial and mouth movements [58,59].”

“At this latency, ERPs are modulated by body and face emotional expressions (Stekelenburg & deGelder, 2004), by comparisons and by encoding of faces with respect to stored individual prototypes (Halit et al., 2000), or by learning semantic associations (Puce et al., 1999).”

“However, evidence that such broader regions are not sufficient for face perception comes from a case of selective loss of face recognition (prosopagnosia) resulting from a very small lesion in just this region [67], and from electrical microstimulation studies that target small regions of cortex and produce selective…”

“More recently, an N200 component for non-face objects was found from sites that extended from the inferior lingual gyrus medially to the middle occipital gyrus laterally (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“For example, Puce, Allison, and McCarthy (1999) measured local field potentials in regions of lateral fusiform cortex in human adults and found that responses of these neurons go from being face selective at around 200 ms after stimulus presentation to being modulated by top-down information such as face identity at l…”

“Consequently, there may also be poor propagation of signal to more frontal regions, which are especially engaged by visual stimuli requiring identification (Bar et al. 2006) and which may serve a top-down feedback role (see also Puce et al. 1999), constraining the function of more posterior regions.”

“, 1994b, 1999), which are modulated by topdown factors such as familiarity and semantic priming (Nobre and McCarthy, 1994; Puce et al., 1999).”

“The latter may be related to the intracranially recorded P350 (Allison et al., 1999; McCarthy, Puce, Belger, & Allison, 1999; Puce et al., 1999), observed anteriorly to the pFs along the ventral temporal cortex.”