Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study

“Twelve normal right-handed subjects (Edinburgh Handedness Inventory range 70 –100) (Oldfield, 1970) without a previous neurological or psychiatric history participated in this study.”

“There are advocates of a unitary system (Damasio et al., 1982; Critchley, 1986; Biederman, 1987), two subsystems dealing with faces and words (Farah, 1990), two subsystems dealing with living and nonliving objects (Sheridan and Humphreys, 1993; Newcombe et al.”

“These results are consistent with the neuropsychology literature (for review, see Rhodes, 1993) demonstrating a right hemisphere advantage for face recognition and with previous PET (Horwitz et al., 1992; Haxby et al., 1995) and scalp-recorded evoked potential (Bentin et al., 1996) studies.”

“Semantic processing of auditorily presented words also activated regions of the temporal lobe distant from ventral cortex (Petersen et al., 1988; Wise et al., 1991; Démonet et al., 1992).”

“Malach et al. (1995) compared the fMRI activation produced by objects (including faces) with the activation produced by textures.”

“It is activated by colors, shapes, and scrambled faces (Corbetta et al., 1991; Clark et al., 1995; Puce et al., 1995a), but not specifically by faces (Table 1) (see also Clark et al., 1995; Puce et al., 1995a).”

“A wide range of noninvasive techniques, including PET, fMRI, ERP, and MEG have shown that FFA responds selectively to images of faces, relative to a wide variety of control objects (1-7).”

“…over other complex visual stimuli such as drawings of objects, faces, and houses (Cohen and Dehaene, 2004; Dehaene and Cohen, 2011; Dehaene et al., 2010; Hasson et al., 2002; Puce et al., 1996; Szwed et al., 2011; Tsapkini and Rapp, 2010 ), thus justifying its ''visual word form area'' label.”

“Both this region and the FFA belong in adults to the visual analysis of faces core system, as defined by Haxby, which also includes the superior temporal sulcus (STS) that is consistently activated in adults (Sergent et al., 1992; Puce et al., 1996; Kanwisher et al., 1997; Chao et al., 1999a,b; Hoffman and Haxby, 2000…”

“…Maps (Lancaster et al., 1997) and (2) use of coordinates of the voxel with the strongest face-sensitive response derived separately from each of five published fMRI studies (Puce et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997; Aguirre et al., 1999; Haxby et al., 1999).”

“The FFA (44, 45) is one of the most intensely studied functional areas of the ventral stream.”

“For example, greater face sensitivity is usually observed in the right hemisphere, while the left ventral pathway exhibits greater sensitivity to written words [122,123], although this lateralization is graded rather than absolute.”

“…processing of objects, such as ventral extrastriate cortex (e.g., Desimone and Ungerleider, 1989; Allison et al., 1994; Haxby et al., 1994; Puce et al., 1996; Lerner et al., 2001), and those involved in maintaining items in memory, such as ventral prefrontal cortex (Bachevalier and…”

“…word forms reliably activates the left fusiform gyrus in a way that other stimuli that control for visual stimulation do not [Price et al., 1997; Puce et al., 1996; Beauregard et al., 1997; Wagner et al., 1998; Brunswick et al., 1999; Fiez et al., 1999; Kiehl et al., 1999; Paulesu et al., 2000;…”

“[2,10,29,31,38,47,54,56].”

“…when contrasting strings of consonants versus strings of pseudoletters (Price et al., 1996a), strings of letters versus checkerboards (Cohen et al., 2002, 2003), or foveal words versus pictures of faces, textures, or buildings (Gauthier et al., 2000; Hasson et al., 2002; Puce et al., 1996).”

“Puce et al. (1996) used fMRI to record neural activity while subjects processed letter strings, faces, and textures.”

“…responds about twice as strongly to faces as to other stimulus categories [Halgren et al., 1999; Kanwisher et al., 1997a; McCarthy et al., 1997; Puce et al., 1996], the parahippocampal place area (PPA) responds selectively to images depicting places [Aguirre et al., 1998; Epstein et al., 1999;…”

“…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 et al. 1996, Tong et al. 1998, Weiner & Grill-Spector 2010).”

“Puce and colleagues and Kanwisher and colleagues (Puce et al., 1996; Kanwisher et al., 1997) described an area in the fusiform gyrus selectively activated by face stimuli (the fusiform face area), while Puce and colleagues (Puce et al., 1998) and Wicker and colleagues (Wicker et al., 1998) have…”

“…voxels [conjunction of (faces chairs) and (faces bodies)] and body-selective voxels (bodies chairs) could be defined separately in LOTC (Puce et al., 1996; Downing et al., 2001) (LOTC-face, LOTC-body) but not in VOTC (Peelen and Downing, 2005; Schwarzlose et al., 2005), where face and…”

“As the right middle FG is a key structure in the processing of face stimuli (Allison et al., 1994; Puce et al., 1995, 1996; Haxby et al., 1996; Kanwisher et al., 1997; Gauthier et al., 2000; Haxby et al., 2001), we investigated whether the functional connectivity of the right middle FG to the rest…”

“…the control session, they referred to studies comparing the processing of faces and bodies, respectively, to that of other kind of materials (i.e., tools, Peelen and Downing, experiment 1, 2005; scrambled controls, Peelen and Downing, experiment 2, 2005; letters or textures, Puce et al., 1996).”

“Activation was also noted in a network of areas implicated in memory retrieval (hippocampus and parahippocampal gyrus) (Maguire, 2001; Schacter and Wagner, 1999; Stark and Sguire, 2000; Yancey and Phelps, 2001) and face recognition (occipitotemporal cortex, including fusiform gyrus) (Clark et al., 1997; Haxby et al.,…”

“…temporal-occipital areas of the left hemisphere than the right hemisphere when contrasted with a baseline consisting of pseudofont characters that otherwise resembled letters in their visual characteristics [Petersen et al., 1990; Price et al., 1994, 1996; Puce et al., 1996; Pugh et al., 1996a].”

“Stable morphological features of the MFS across children, adolescents, and adults In the original observation of the MFS in modern writing, Puce et al. (1996) reported, “The fusiform gyrus often is divided by a longitudinal sulcus that can be confusedwith the collateral sulcus in isolated coronal…”

“…studies by faces (often bilaterally but more reliably on the right than on the left) when contrasted with other objects or scrambled images [Puce et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997], can be modulated by attention under some conditions [Haxby et al., 1994], and may…”

“Puce, Allison, Asgari, Gore, and McCarthy (1996) measured the hemodynamic response with functional magnetic resonance imaging (fMRI) when subjects viewed unfamiliar faces, letter strings (unpronounceable nonwords), and textures.,How may results such as those of Puce et al. (1996) be reconciled with this conclusion? Pu…”

“Recent neuroimaging studies using positron emission tomography (Sergent et al., 1992; Haxby et al., 1994) and functional MRI (Puce et al., 1995, 1996; McCarthy et al., 1997) have demonstrated that regions of ventral occipitotemporal cortex are activated reliably by faces ± particularly within the fusiform gyrus.”

“The Petersen study has since been followed by a number of other imaging experiments, most of which were PET studies, aimed at differentiating among components, such as lexical analysis, phonology, and semantics in visual single-word processing (Indefrey et al., 1997; Rumsey et al., 1997; Puce, Allison, Asgeri, Gore, &…”

“…has been reported in the posterior ventral temporal cortex for human faces, four-legged animals, tools, houses/buildings, letter strings and chairs (Puce et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997; Aguirre et al., 1998; Epstein and Kanwisher, 1998; Chao et al., 1999a,b; Haxby et…”

“We did not set out to examine the functional anatomy of facial processing per se, which would have required contrasting faces with, for example, other visual objects or scrambled faces Žsee Puce et al., 1995, 1996; Kanwisher et al., .”

“For example, an area in the posterior fusiform gyrus is specialized for colour (human area V4: Zeki et al., 1991; McKeefry and Zeki, 1997), a ventrolateral area is specialized for motion (human area V5: Watson et al., 1993) and an area anterior to V4 is specialized for faces (Puce et al., 1996).”

“, 1997), the occipital face area (OFA) (Gauthier et al., 2000; Puce et al., 1996), the STS and theAMG(Haxby et al.”

“Despite the fact that several imaging studies have nvestigated the specificity of face processing as comared to other objects (Puce et al., 1996; Kanwisher et l., 1997b; McCarthy et al., 1997), the encoding and the ecognition of faces (Kapur et al., 1995; Haxby et al., p 279FUNCTIONAL NEUROANATOMY…”

“The lingual gyrus has been implicated in higher-order processing of visual information (52,53), speci fi cally in early stages of face processing (54).”

“Face-selective neural responses have been observed using functional magnetic resonance imaging (fMRI) in several regions of the human occipitotemporal cortex, including the posterior inferior occipital lobe (Puce et al., 1996), posterior superior temporal sulcus (Allison et al.”

“Occipitotemporal face-speci®c activation can be seen bilaterally, but generally with at least slight right-hemisphere (RH) dominance (e.g. Sergent et al., 1992; Haxby et al., 1994; Bentin et al., 1996; Puce et al., 1996; Kanwisher et al., 1997; Sams et al., 1997; GornoTempini et al., 1998; Swithenby et al., 1998; Halg…”

“& Farah, 1995; Polk et al., 2002; Puce, Allison, Asgari, Gore, & McCarthy, 1996 ).”

“Cortex around the collateral sulcus has a relative specialisation for textured patterns (Puce et al., 1996) while area V2 (located in the lingual gyrus and cuneus) has been linked to grid and brickwork hallucinations in eye disease (Burke, 2002).”

“In typically developing individuals, the fusiform area (FA) has been associated with the perceptual processing of faces (Clark et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997; Puce et al., 1996; Tarr and Gauthier, 2000) and with the attribution of emotion from basic facial expressions (Critchley et al.”

“…and happiness, and to facial expressions of low-intensity sadness contrasted with neutral facial expressions, activation within the fusiform gyrus, an extrastriate cortical region important for facial and object processing (Haxby et al., 1994; 2000; Puce et al., 1995; 1996; Kanwisher et al., 1997).”

“Neuropsychology, direct electrical recordings (Allison et al., 1999; Bentin et al., 2002), and neuroimaging (Sergent and Signoret , 1992; Haxby et al., 1996; Puce et al., 1996) all suggest that a specific region in the fusiform gyrus responds selectively to images of faces.”

“Intent judgements are assigned to pSTS/the temporal parietal junction (TPJ), consistent with what is generally known about the role of these areas in social cognition (cf. Haxby et al., 2000; Puce et al., 1996).”

“Cerebral Cortex May 2008, V 18 N 5 1003 Consistent with a large literature (Sergent et al. 1992; Allison, Ginter et al. 1994; Allison et al. 1999; Puce et al. 1996; Kanwisher et al. 1997; McCarthy et al. 1999; Haxby et al. 1999; Rossion et al. 2000; Ishai et al. 2005), these data demonstrate that…”

“Activations evoked by line textures, which have been shown to activate ventral occipitotemporal areas (Beason-Held et al. 1998; Gulyas et al. 1998; Puce et al. 1996), were studied when presented as uniform textures compared with segregated textures containing boundaries that formed a checkerboard…”

“…predominantly right hemispheric lateralization of other visual body and face selective regions, such as FBA (Peelen and Downing 2005), FFA (Kanwisher et al. 1997), OFA (Puce et al. 1996), and EBA itself (Downing et al. 2001), the hand response in LOS showed a strong left hemispheric lateralization.”

“, 1994a,b) and fMRI studies (Clark et al., 1995; Sabbah et al., 1995; Puce et al., 1996; Kanwisher et al., 1997), whatever the task realized.”

“…processing), healthy controls and schizophrenia patients showed a general pattern of brain activation to faces consistent with previous research (Puce et al., 1996; Phillips et al., 1998; Sprengelmeyer et al., 1998; Swithenby et al., 1998; Halgren et al., 1999; Gorno-Tempini et al., 2001;…”

“Previous neuroimaging studies suggest a crucial role for the right anterior temporal cortex in facial emotional expression and recognition [12,13,21] and emotional response in healthy women (primarily when induced by film) [7].”

“Studies addressing this possibility have provided conflicting evidence: several human [2-6] and animal studies [7] found stronger activity in the right hemisphere, while other studies failed to support the notion of a strict right-lateralization (e.”

“…Roman letters, in comparison with digit and Chinese character controls, suggests specialization that cannot be explained by simple shape differences such as those between letter strings and complex stimuli (e.g., faces or textures used in other studies; see Hasson et al., 2002; Puce et al., 1996).”

“Perception of still images of faces and objects evokes neural activity primarily in early visual cortices and in the extrastriate cortices of the ventral object vision pathway (Puce et al. 1996; Kanwisher et al. 1997; Haxby et al. 1999, 2001; Ishai et al. 1999, 2000).”

“…face processing have reported stronger responses to faces than to other categories of objects in the fusiform face area (FFA, Sergent et al. 1992; Puce et al. 1995, 1996; Kanwisher et al. 1997), the occipital face area (OFA; Kanwisher et al. 1997; Gauthier et al. 2000), and the right ATL…”

“In humans, faces selectively activate the mid fusiform gyrus (Kanwisher et al., 1997), the lateral occipital cortex (Puce et al., 1996), the anterior and posterior regions of the superior temporal sulcus (Puce et al., 1998; Pitcher et al., 2011), and the anterior portion of the inferotemporal…”

“…the identification of objects in general would have species-specific survival value worth the allocation of neural resources and specialization by categories and their attributes has been demonstrated (Ishai et al., 1999, 2000; Martin et al., 1996; McCandliss et al., 2003, 1995; Puce et al., 1996).”

“With the present systematic comparison we observe a main effect of fearful expression in the right inferior occipital gyrus, a location comparable to that of the occipital face area (Allison et al., 2000; Puce et al., 1996).”

“These results indicate, as has been proposed by other researchers (e.g., Puce et al., 1996), that orthographic and object stimuli produce distinctive patterns of neural activity.”

“However, lateral temporal cortex is also active when subjects view static faces (Puce et al., 1995, 1996, 1997), so the functional significance of this region as yet remains undetermined.”

“, 2002 ), textures ( Puce et al., 1996), faces ( Gauthier et al.”

“, 1992) and humans (Puce et al., 1996; Allison et al., 1999), we chose as the most likely candidate for Source 3.”