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

“The N200 was generated in the ventral and lateral face areas and was active during face perception but was not elicited by affective stimuli, diminished by habituation, affected by familiarity of the face, nor affected by semantic priming or face naming (Puce et al., 1999).”

“Similarly, intracranial recordings failed to reveal top-down modulation of the N200 to faces (Puce et al., 1999).”

“…are observed in humans using neuroimaging (e.g., Gauthier et al., 2000; Haxby et al., 2000; Kanwisher et al., 1997; Puce et al., 1995; Rossion et al., 2000; Sergent et al., 1992) and field potential recordings on the cortical surface (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“Scalp ERP studies and intracranial recordings indicate that early visual components (below 250 msec) are not influenced by face familiarity (Bentin & Deouell, 2000; Eimer, 2000; Paller et al., 2000; Puce et al., 1999; Rossion et al., 1999) and thus preferentially support this last hypothesis.”

“…with the involvement of a lateral source also found in some fMRI studies around the superior temporal sulcus (STS) region (Ishai et al., 2005; Puce et al., 1995) and with intracranial recordings of the face-specific component N200 (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“…a number of studies have found that the N170 does not discriminate between famous faces and unknown faces (Bentin & Deouell, 2000; Eimer, 2000; Puce et al., 1999; Zion-Golumbic & Bentin, 2007, but see Latinus, Bayle, Deltheil, Bohler, & Taylor, under review), and that discrimination of…”

“Many studies have recorded face-specific or face-sensitive potentials around that latency in the fusiform gyrus (N200: Allison et al., 1994, 1999; P180: Halgren et al., 1994; N200: McCarthy et al., 1999; Puce et al., 1999; N160: Mundel et al., 2003; P160: Barbeau et al., 2008), including one study with fMRI functional…”

“(16) reported the perception of faces and face parts after stimulation of the fusiform gyrus], it is unknown whether the complexity of stimulation-induced percepts changes systematically across visual areas.”

“These studies have shown that electrical stimulation of LOC in epileptic patients, implanted with electrodes for seizure focus localization, interferes with object recognition (Puce et al., 1999) and that lesions of these regions produce deficits in object recognition (Damasio et al.”

“Previous ERPs elicited to static isolated faces appear to have two generator sources, as indicated by intracranial recordings made from the surface of temporo-occipital cortex (e.g., Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“In previous work on humans the N200 has been associated with face processing and visual attention ( Allison, Puce, Spencer, & McCarthy, 1999a,1999b ).”

“Intracranial recordings reveal a face-specific response 200 ms after stimulus onset (N200) as was first reported by Allison et al. (1999), McCarthyet al. (1999) and Puce et al. (1999).”

“Because the N170 effect is enhanced rather than reduced by face inversion (Rossion et al., 1999, 2000), it is not sensitive to face familiarity (Bentin & Deouell, 2000), and it is elicited by isolated face parts (particularly eyes) as well as by full face-gestalts, Bentin and his collaborators suggested that the N170…”

“, 1989), most recordings from the human hippocampus have not demonstrated learning-related ERP changes (Nobre and McCarthy, 1995; Puce et al., 1999).”

“Although evidence exists for short-term habituation of early ERP components ( Woods & Elmasian, 1986), recent studies suggest that the N170 may not be susceptible to habituation ( Puce, Allison, & McCarthy, 1999 ).”

“The AUC from our ROC analysis reached almost 1 in both epochs (Figure 6D, maximum AUC of 0.99 for static and 0.99 for dynamic), demonstrating that maximum ERBPs from single trials can almost perfectly distinguish responses to faces from those to control checkerboards.”

“…or moving objects (Rauschecker et al. 2011, Richer et al. 1991), complex objects such as faces or face parts ( Jonas et al. 2014a, Lee et al. 2000, Puce et al. 1999), or hallucinations of visual scenes that the patient is familiar with (Figure 11b) (Megevand et al. 2014). www.annualreviews.org •…”

“Arguably the best combination of large anatomical field-of-view, good spatial resolution, excellent temporal resolution, and wide frequency bandwidth, is afforded by field potentials, which can be recorded in awake neurosurgical subjects [1–4,6–8,41–44].”

“[25,26,31,49,56]) studies suggest that the fusiform is specialized for face and/or object perception.”

“At the physiological level, the neural systems mediating face perception have been widely examined in a number of studies using functional neuroimaging techniques (review in Haxby, Hoffman, & Gobbini, 2000; Kanwisher, 2000; McCarthy, 1999) and human electrophysiology (Allison, Ginter, et al., 1994; Allison, Puce, Spen…”

“Earlier potentials such as the face-sensitive N170 (Bentin et al. 1996; Puce et al. 1999) did not differ between conditions .”

“Puce et al. (1999) addressed the issue of emantic (identity) priming on intracranial event-reated potential (ERP) study.”

“Support for VLPFC involvement in object and face processing is apparent in neuroimaging studies of the human brain (Allison, Puce, Spencer, & McCarthy, 1999, Courtney, Ungerleider, Keil, & Haxby, 1996, 1997; Haxby et al., 1996; McCarthy et al., 1996; Puce, Allison, & McCarthy, 1999 ).”

“An intriguing puzzle in memory research is that cortical representations of event contents, such as faces, emerge very rapidly, within 200 ms (McCarthy et al., 1999; Puce et al., 1999; Fisch et al., 2009; Rossion and Caharel, 2011), whereas encoding processes in brain regions that are critical for recollection (i.”

“Previous studies of evoked potential using humans have suggested an early separation of face and gaze signals in the processing streams used for face perception (Allison et al. 1999; McCarthy et al. 1999; Puce et al. 1999; Shibata et al. 2002).”

“One previous study using intracranial event-related potential (ERP) reported that the first distinct response in visual ventral areas appears 200 msec after the stimulus onset (Puce et al., 1999).”

“…Glasgow, 58 Hillhead Street, Glasgow, G12 8QB, UK. e-mail: guillaume.rousselet@glasgow. ac.uk www.frontiersin.org May 2011 | Volume 2 | Article 107 | 1 PersPective Article published: 23 May 2011 doi: 10.3389/fpsyg.2011.00107 described as a specific response from a face module (Puce et al., 1999).”

“Indeed, an early case study using this approach (Puce et al., 1999) reported that ventral temporal stimulation near the likely location of the fusiform body area evoked the percept of a human body.”

“This hypothesis is consistent with electrophysiological data recorded intracranially from neuropsychological patients that shows a range of face tasks generate event-related potentials with the same latencies in both the ventral and lateral occipitotemporal cortices (Allison et al., 1999; McCarthy et al., 1999; Puce e…”

“Face selective brain regions are found throughout the posterior and anterior fusiform (Allison et al., 1999; Puce et al., 1999; Tsao et al., 2008; Rajimehr et al., 2009; Ku et al., 2011; Nsar and Tootell, 2012; Tanji et al., 2012), suggesting that visual analysis of faces continues beyond the FFA.”

“Depth and cortical electrode studies in humans have recorded face-specific activity in the ventral temporal and frontal lobes (Halgren et al., 1994; Puce et al., 1999).”

“…on monkey cell recordings (Perrett et al., 1982; Perrett et al., 1985) and human intracranial data (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999), assumes that eye and face selective neurons co-exist in the human brain and that their differential response patterns to various…”

“In humans, regions involved in visual recognition have also been observed to produce a relatively reduced cortical response for repeated stimuli, as measured in studies using positron emission tomography (PET, Badgaiyan et al., 2001; Buckner et al., 1995), event related potentials (ERP, Puce et al., 1999; Rugg et al.…”

“…investigations that have reported a facespecific N200 from electrodes situated mainly at ventral occipitotemporal sites [Allison et al., 1994, 1999; Puce et al., 1999], and ERP studies describing the earliest response to faces at around 170 msec, the so-called N170, characterised by a…”

“We have previously suggested on the basis of ERP recordings made directly from ventral temporal cortex that there may be a temporal dimension to modular processing (Puce et al., 1999).”

“For example, results showing no early effects of face repetition (e.g., Puce et al., 1999; Schweinberger et al., 2002b) using relatively long ISIs (∼ 2 s) are actually entirely compatible with findings showing early effects of repetition (e.g., Harris and Nakayama, 2007b; Jeffreys, 1996; Kovacs et…”

“Cerebral Cortex May 2011;21:1213--1221 doi:10.1093/cercor/bhq206 Advance Access publication October 20, 2010”

“, 1997) and intracranial recording (Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999) studies demonstrating that regions of the anterior fusiform gyrus in both hemispheres exhibit more robust responses to faces compared to other categories of stimuli.”

“Face-N200 is largely insensitive to face repetition and to higher cognitive task manipulations, and this insensitivity has led to the proposal that face-N200 reflects an initial and obligatory neural response to faces (McCarthy et al., 1999; Puce et al., 1999).”

“…regarding the functional properties of these areas derived from fMRI research (Grill-Spector and Malach, 2004), as well as previous iEEG studies (Puce et al., 1999), suggests that high-level visual representations likely include holistic aspects of the objects rather than low-level features…”

“We mentioned already evidence about face selective cells from animal studies (Ashbridge, Perrett, Oram, & Jellema, 2000) and human electro-physiology (Puce et al., 1999).”

“Face perception induces the N170 component in the occipito-temporal cortex, mainly in the fusiform gyrus [7,32–42].”

“…to comparing mental imagery of these two categories is that faces and objects recruit different posterior visual processing areas (Hasson et al., 2003; Downing et al., 2006) and are associated with distinct ERP signatures (e.g., Schendan et al., 1998; Allison et al., 1999; Puce et al., 1999).”

“Category-Sensitive Excitatory and Inhibitory Processes in Human Extrastriate Cortex”

“This interpretation is consistent with intracranial ERP recordings showing that while the N200 is insensitive to attention and task demands, longer latency components may be modulated by top–down processing (Puce et al., 1999).”

“Interestingly , intermediate components such as face specific N200 are insensitive to a wide variety of top-down processes (Puce et al., 1999).”

“…modulation of face categorization by electrical stimulation of the monkey infero-temporal cortex), impairment in face naming (Allison et al., 1994; Puce et al., 1999) or distortions of the physician's face following electrical stimulation of other faceselective regions (Parvizi et al., 2012;…”

“1994, 1999 ; McCarthy et al., 1999; Puce et al., 1999 ) and further neuroimaging studies (Gauthier et al., 1999, is a”

“P290, P350) appear to receive taskrelated top-down modulatory inputs from the frontal regions (Puce et al., 1999).”

“16) of three kinds of oddball stimulus were evaluated before the main task with significant difference across them (F (2,87) = 602.”

“…areas (Nobre et al., 1994) and it has been suggested that these brain areas could accommodate ensembles of neurons specialized in the recognition of letters, graphemes or words, and that they are likely to be intermixed with other neurons involved in object and face recognition (Puce et al., 1999).”

“We have proposed that the face-specific N200 generated in the FG is an obligatory response to faces, which accounts for its general insensitivity when challenged with cognitive and perceptual manipulations [Allison et al., 1999; Engell and McCarthy, 2010, 2011; Puce et al., 1999].”

“Stimulations of the temporal lobe evoked either complex hallucinations [Ishibashi et al., 1964, Lee et al., 2000, Puce et al., 1999], visual illusions [Lee et al., 2000], or no detectable percept or elementary hallucinations [Murphey et al., 2009].”

“, typical sequence of P150/N200/P290 waveforms, followed by a prolonged N700) between our findings (see Figure 3) and earlier intracranial ERP results obtained in other epileptic patients (see Allison et al., 1999; McCarthy et al., 1999; Puce et al., 1999).”

“The earliest face-specific evoked potential—not driven by low-level features—peaks at around 170ms from stimulus onset (the N170 in EEG [13,53–55] and the M170 in MEG [48,49].”

“Further, occipitotemporal cortex, where the intracranial N200 is recorded, also shows later P290 and N700 waves that may reflect re-entrant input to the same cells (Allison et al., 1999, 2002; Puce et al., 1999), consistent with an interactive state 2 during the N3.”

“The STS receives axons from and sends projections into the amygdala and the VLPFC (Rolls, 2000; Puce, Allison, & McCarthy, 1999 ).”

“Possible Relation of the Attentional Modulation to the N200 The early attentional modulation of face processing peaks at 208 ms. This suggests a possible link to the face-specific N200 characterized in intracranial recordings from occipitotemporal cortex (Allison, Puce, Spencer, & McCarthy, 1999; McCarthy, Puce, Belge…”

“For example, subdural electrical recordings (Allison, Puce, Spencer, & McCarthy, 1999; McCarthy, Puce, Belger, & Allison, 1999; Puce, Allison, & McCarthy, 1999; Allison, Ginter, et al., 1994) and functional neuroimaging studies (Grill-Spector, Knouf, & Kanwisher, 2004; Kanwisher, McDermott, & Chun, 1997; McCarthy, Puc…”

“The N170 component is sensitive to a range of manipulations of faces [29-32] suggesting that it reflects automatic face processing [33,34].”