Hemispheric specialization of cognitive function in typical adult brain is well documented. One well-known example is the lateralization of language in the left hemisphere, perisylvian areas dedicated to language processing being functionally (see Tzourio et al., 1998; Celsis et al., 1999, for examples) as well as anatomically (Geschwind and Levitsky, 1968; Foundas et al., 1995) left lateralized in the great majority of right-handed subjects. Conversely visuo-spatial and face processing abilities would be lateralized toward the right hemisphere. This right hemisphere dominance for face processing has been originally demonstrated, thanks to prosopagnosic patients – patients showing specific inability to recognize faces following brain damage. Indeed, although prosopagnosics generally suffer from bilateral lesions, a right hemisphere lesion seems sufficient to produce significant impairments in face recognition (De Renzi, 1986; De Renzi et al., 1991). The hypothesis of a right hemisphere advantage for face processing is also supported by fMRI results, showing a functional asymmetry in favor of the right hemisphere during face processing, particularly in the Fusiform Face Area (FFA; Badzakova-Trajkov et al., 2010; Rossion et al., 2012; Bukowski et al., 2013).

At the behavioral level, this right hemisphere dominance for face processing is thought to be the cause of a left visual field (LVF) bias, the fact that facial information present in the LVF is crucial for categorization and recognition (Levy et al., 1983; Luh et al., 1991; Burt and Perrett, 1997). Burt and Perrett (1997), for example, used chimeric faces (faces vertically split in two different halves) to assess right hemisphere advantage during the detection of variable face attributes, such as gender, age or facial expression. The stimuli presented to participants were composed of two average half faces (e.g., left half is an average of male faces whereas right half is an average of female faces) with the join down the center blended rendering it invisible to participants. The rationale beyond this image manipulation is that the left and right hemispheres receive respectively the right and left part of the image relative to the point of foveation. Gazing three degree to the right of a face will place the entire image in the LVF and this signal, conveyed through the right visual tract, will be first processed in the right hemisphere. Acuity drops drastically with eccentricity from point of foveation and we generally look directly at faces to access to more details. Nevertheless, when we fixate different locations in a face, the left and right hemisphere are processing only partly overlapping right and left parts of the face. Burt and Perrett (1997) found that participants’ judgments of gender and expression were influenced to a greater extent by the information on the left of the face from the viewer’s perspective. This finding has been largely replicated (Butler and Harvey, 2005; Butler and Harvey, 2008; Yovel et al., 2008; Bourne and Gray, 2011). To establish a straight relationship between hemispheric lateralization and the LVF bias obtained using chimeric faces, Yovel et al. (2008) used fMRI while participants performed a matching task. Participants were presented chimeric faces in the scanner, and also performed the same task outside the scanner. The resulting activity in the FFA was rightward asymmetric, and this asymmetry was positively correlated with the LVF bias obtained from the behavioral test ran outside the scanner. This confirmed that the LVF bias obtained using chimeric faces does, at least in part reflect right hemispheric specialization of face processing areas. Right hemisphere advantage for the processing of face could be related to the processing of configural information in face (Schiltz and Rossion, 2006; Maurer et al., 2007), right hemisphere being generally thought to process predominantly global information whereas left hemisphere would be specialized in the processing of local information (Fink et al., 1996, 1999; Lux et al., 2004).

The relative contribution of right hemisphere lateralization and attentional factors resulting from the scanning patterns in the LVF bias is, however, not fully understood. An increased LVF bias in trials in which participants spent more time looking at the left part of the face suggests a clear link between attentional factors resulting from scanning patterns and the LVF bias (Butler et al., 2005). However, this bias can be observed even with short presentation times (100 ms) that are preventing eye movements, ruling out the effect of purely attentional factors (Butler and Harvey, 2006, 2008). The presence or absence of a LVF bias would thus result from a complex interplay between bottom-up perceptual processing factors and top–down attentional factors which could be both lateralized, similarly to what has been suggested for written language (Selpien et al., 2015).

The LVF bias is also robustly found even with line drawing (Luh et al., 1991), or inverted stimuli (Butler and Harvey, 2005). Using chimeric faces, Aljuhanay et al. (2010) found that the LVF bias was present as early as 5 years of age. The root of the hemispheric asymmetry in face processing has been hypothesized to lie in the development of the hemispheric specialization. Infants recognize a face faster if it is initially presented in the LVF as opposed to the right visual field (de Schonen and Mathivet, 1990). This processing bias may represent the precursor of the asymmetry observed in adults.

If the brain asymmetry for face processing emerges during development, early deprivation or dramatic differences the infant experiences with the world should affect it. For example, 9- to 23-year-old participants treated for bilateral congenital cataracts after 7 weeks of age, who were deprived of patterned visual input during this duration, fail to develop some of the aspects associated with typical adult levels of face recognition such as the face composite effect suggesting impaired configural processing (Le Grand et al., 2001). This emphasizes the importance of early visual experience in the development of adult face processing abilities. Cross-modal interactions have also been found to affect visual development; for example early auditory deprivation has been shown to affect the development of some visual abilities. Several studies showed that deaf participants could detect targets at larger eccentricities, indicating larger visual field (Buckley et al., 2010; Codina et al., 2011). Better abilities have also been found in deaf participants for the detection of motion in the visual periphery (Armstrong et al., 2002; Bosworth and Dobkins, 2002; Stevens and Neville, 2006; Hauthal et al., 2013). The observation of enhanced processing in the periphery, particularly under attentional conditions, seems very reliable in the literature (Parasnis and Samar, 1985; Neville and Lawson, 1987; Bavelier et al., 2000, 2001; Bottari et al., 2010). Higher-level visual abilities have also been shown to be modified by early deafness, such as visual imagery (Emmorey et al., 1993, 1998) or the processing of faces (Bettger et al., 1997; Arnold and Murray, 1998). Using the Benton Test of Facial Recognition, Bettger et al. (1997) tested the recognition of individual faces in deaf participants. They obtained better scores than hearing non signers, but only in a difficult condition, in which faces were shadowed. This enhanced processing in deaf people could thus concern very particular aspects of face processing; McCullough and Emmorey (1997) found that deaf and hearing participants differed only by the detection of subtle facial features. Feature analysis relates to configural face processing and de Heering et al. (2012) suggested an increased dependency on this mode of processing in deaf participants.

If visual processing is affected by early deafness, what about visual asymmetries? Several experimental studies examining hemispheric asymmetry in congenitally deaf individuals found that it differs from the one observed in hearing individuals (Szelag and Wasilewski, 1992; Szelag, 1996; Neville et al., 1997). As for the processing of sign language, an extensive amount of data show that it could activate the typical left-lateralized speech processing network (Pettito et al., 2000; MacSweeney et al., 2002, 2008). However, other studies suggest greater contribution of the right hemisphere for the processing of sign language than for spoken language (Neville et al., 1997, 1998; Emmorey et al., 2002). In addition damage to both left and right hemisphere lead to language deficit in sign language users (Corina and McBurney, 2001). Neville and colleagues proposed that greater recruitment of right hemisphere would be related to the visual-spatial characteristics of sign language. However, recent results suggest a reduction of hemispheric lateralization in a spatial attention task (Cattaneo et al., 2014). A shift of hemispheric lateralization during the detection of motion has also been demonstrated, deaf subjects showing a left hemisphere advantage, whereas hearing subjects showed a right hemisphere advantage (Bosworth and Dobkins, 1999; Bavelier et al., 2001; Bosworth et al., 2013). The question of cerebral lateralization for sign language processing results from a complex interplay between language-related and other cognitive – visuo-spatial, gestural, motion-related – functions modulated by sensory experience that are still poorly understood.

With regard to face processing, few studies investigated hemispheric lateralization during the perception of faces in deaf people and the results are rather contrasted. Phippard (1977) presented briefly unfamiliar faces in either the left or right visual field and found no differences between deaf and hearing participants. More recently Letourneau and Mitchell (2013) found a typical LVF asymmetry during an identity judgment task. Neurophysiological studies suggest a reduced right hemisphere asymmetry in deaf participants compared with hearing ones (Weisberg et al., 2012; Mitchell et al., 2013). Mitchell et al. (2013) for example found a reduced asymmetry of the neural responses to neutral faces around 200 ms in deaf participants when compared with the hearing group. Other studies principally focused on the processing of emotional and/or linguistic facial expressions. Indeed, although facial expressions are a universal cue to recognize the emotional state of individuals, sign language users must also recognize facial expressions as linguistic markers which could affect the hemispheric lateralization. Concerning emotional expressions, Szelag and Wasilewski (1992) presented emotional (happy, sad) and non-emotional faces in the left or right visual field in deaf children. They found a LVF (right hemisphere) advantage for neutral and sad faces in normal hearing, and no hemispheric advantage for any kind of faces in deaf participants. More recently, Letourneau and Mitchell (2013) found a reduction of the LVF bias during an emotion judgment task in deaf participants. Corina (1989) investigated the LVF advantage for affective and linguistic facial expressions; they obtained a reduced LVF bias in deaf participants for both types of expressions, but this was strongly affected by the order of presentation. A following study (Corina et al., 1999) suggests that the cerebral lateralization for facial expression could depend on the functional role (linguistic/affective) of these expressions. Finally, McCullough et al. (2005), using fMRI, investigated cerebral asymmetries during the presentation of linguistic or emotional facial expressions. For emotional expressions, they found a right hemisphere lateralization in the STS in hearing controls, whereas activation was symmetrical in deaf participants. For linguistic facial expressions, activation was also right lateralized in hearing subjects, but left lateralized in deaf participants. Some modifications of the asymmetry for emotional and linguistic facial expressions were also observed in the fusiform gyrus, where hearings exhibited a slight rightward asymmetry for both types of expressions, whereas activity was leftward lateralized in deaf participants (see also Emmorey and McCullough, 2009).

Taken together, these results suggest differences of the functional hemispheric asymmetry for the processing of both linguistic and emotional expressions. However, it still unclear whether this plasticity extends to the core aspects of face processing. By presenting neutral faces, Weisberg et al. (2012) found a reduced activity in the right fusiform gyrus in deaf participants in comparison with hearing non signers, whereas no difference was observed in left fusiform. This could suggest reduced asymmetry in deaf participants. However, this study being not designed to investigate cerebral asymmetry, it remains difficult to draw firm conclusion about hemispheric lateralization in deaf participants.

Our review of the literature suggests the existence of some modifications in the cerebral asymmetries in deaf people, resulting either from auditory deprivation or/and their extensive use of sign language. Concerning facial processing, these modifications are less well established. To date, evidences for modifications of hemispheric lateralization for the processing of neutral faces are rather scarce and it is unclear how deafness affects the processing of invariant aspects of face. The present experiments are interested in examining the LVF bias in a population of deaf adults and non-signer hearings. We used a gender recognition task with chimeric faces. Assuming that LVF bias reflects right hemispheric dominance for face processing we predicted a reduced LVF bias in deaf participants. From the results of Weisberg et al. (2012), this reduced LVF bias would be linked to a reduced activity in the right fusiform gyrus during face processing. This hypothesis was tested in Experiments 1 and 2. In Experiment 2 we also measured eye movements during face scanning to investigate the consequences of early auditory deprivation on the visual attention toward face features in the gender recognition task.

An established fact in perceptual asymmetries is that for many aspects of face identity processing (perception of age, attractiveness, gender or expression) typical individuals attend to information on the right side of the face, leading to a LVF bias (Burt and Perrett, 1997; Butler and Harvey, 2005). This left bias is thought to reflect a right hemisphere advantage for face processing (Yovel et al., 2008). In deaf people, auditory deprivation and use of sign language seem to affect hemispheric lateralization (Bosworth and Dobkins, 1999; Bavelier et al., 2001). To date, very few studies have found modifications of lateralization using face stimuli in deaf people, and only for the processing of facial expressions (McCullough et al., 2005; Letourneau and Mitchell, 2013). The present study is the first to specifically investigate visual field asymmetries for the processing of facial identity using chimeric faces in deaf people. Using a gender categorization task we found that it was less frequent to find a significant LVF in a group of early deaf participants than in hearing controls. This suggests modifications of cerebral lateralization in deaf people for the processing of invariant aspects of faces, suggesting that early deafness, together with the extensive use of signed language, affects not only the processing of facial expressions, but also the core mechanisms underlying face recognition. Our results are in agreement with those obtained by Szelag and Wasilewski (1992), who found using a divided visual field task a reduced LVF bias in congenital deaf children. In their study this absence of visual field advantage seemed to come from a more variable asymmetry in deaf children, with approximately half of deaf children showing a leftward asymmetry and the other half showing a rightward asymmetry. This variability is also present in our experiments where a clear LVF bias was found in fewer deaf participants than in the hearings. This suggests a greater variability in face hemispheric lateralization in deaf people, potentially resulting from an increased role of the left hemisphere relatively to the right.

This variability may be explained by the heterogeneity of the deaf sample; as shown in Table 1 our deaf participants differ in terms of etiology of deafness, learning age and daily use of sign language, lip reading abilities or the daily use of hearing aid. This heterogeneity may have influenced our results, and can explain a greater variability in terms of brain specialization. In particular the principal language used in the daily life (oral vs. signed) as well as the age of acquisition of sign language could greatly influence the development of visual field asymmetries. It would be of interest to study more directly the impact of sign language in visual field asymmetries for face processing. Another important point to consider is lip-reading ability, as shown by our post hoc analysis; there is a negative correlation between fixation time on the mouth area and the amount of left visual bias. It indicates that paying more attention toward the mouth reduces the LVF asymmetries, because it draws attention toward of the center of the face.

The question that arises from our present results is why deafness would affect face processing. One possibility is that during infancy, children have to learn to link auditory and visual inputs to form one unique perceptual object. To identify a person in everyday life, we rely indeed not only on visual processing of faces, but also on the processing of vocal information. In the absence of the auditory modality, visual processing of face should thus become more salient for communication and social interactions. Another possibility is that face processing is influenced by the use of sign language whereby facial expressions convey information about the emotional state of individuals, but also carry linguistic information. Thus, deaf signers have to pay attention to face for both affective and linguistic inputs; it seems thus possible that they develop particular processing mechanisms that allow them to maximize the ability to gather information from faces. Shifts of cerebral lateralization for the processing of facial expressions from right to left have been observed in deaf participants for the processing of facial expressions (Emmorey and McCullough, 2009) and some results show that right hemisphere activation could be reduced for the processing of neutral faces (Weisberg et al., 2012). Interestingly enough, Weisberg et al.’s (2012) results seem to indicate joint effects of auditory deprivation and extensive use of sign language on cerebral activation. To disentangle these two effects, they also tested a group of hearing signers. Activation in the right middle fusiform gyrus for this group was at an intermediate level between deaf signers and hearing non-signers, suggesting a combined effect of the sensory deprivation and use of sign language. However, this study was not specifically designed to test cerebral asymmetry for face processing in deaf, thus additional studies are needed to evaluate more precisely how asymmetry for face processing is modulated by auditory deprivation.

One limitation of our study is that we did not test a group of hearing signers; therefore the question of whether the modifications of visual field asymmetries observed in this study are related to auditory deprivation, expertise with sign language, or a combination of both, remains open. To disentangle the relative influences of sensory deprivation and plasticity resulting from the use of sign language, it will be necessary to investigate asymmetry using chimeric faces in a population of native hearing signers.

One purpose of the present study was to relate the amount of LVF in deaf participants with the left/right scanning behavior of the participants. Previous studies suggest indeed that the LVF bias results not only from a right hemisphere advantage during face processing, but also from the scanning pattern of participants favoring the inspection of the left side of the face. The left side of the face would be investigated first, and longer than the right side (Phillips and David, 1997; Butler et al., 2005; Guo et al., 2012). The LVF bias has been found to be reduced in people who have a reversed scanning pattern such as Hebrew or Arabic readers (Vaid and Singh, 1989; Heath et al., 2005). The reduction of the LVF bias in deaf people could thus come from a reduction of cerebral asymmetry in face areas, from a scanning pattern favoring more the right side of the face, or both. Early deafness has been found to affect the pattern of eye movements (Watanabe et al., 2011; Bottari et al., 2012), even in non-linguistic or non-emotional tasks, suggesting that the habitual gazing pattern toward faces is altered in deaf people. In our study, we found no left/right difference in the scanning patterns of our participants, but there was a difference in the bottom/up repartition of fixations. While deaf participants showed the classical fixation pattern eyes-mouth-nose like hearing controls, the proportion of fixations on the mouth was increased in deaf participants as costs of attention to the eyes. This suggests a tendency in deaf participants to favor more the information contained in the mouth than hearing participants even in non-communication situations. Alterations of gazing behavior in communication situation have been suggested before (Emmorey et al., 2009). In this study the authors found that in a communication situation, beginning ASL signers fixated more the mouth than native deaf ASL signers who fixated preferentially the eyes. Interestingly enough, other results indicate that these alterations of the gazing behavior could extend to the perception of static faces (Letourneau and Mitchell, 2011; Watanabe et al., 2011). Watanabe et al. (2011) used static faces in early deaf and hearing participants and found an increased fixation time on the eyes in the deaf group relatively to the hearing group. This seems at odd with our results, however, this discrepancy can be explain by cultural bias; Watanabe et al.’s (2011) results have been obtained in Japanese participants which makes the comparison difficult to draw as East Asian observers fixate less the eyes than Western Caucasians (Blais et al., 2008; Miellet et al., 2013). In agreement with our results, another recent study (Mitchell et al., 2013) using composite neutral faces showed an increased attention to the bottom of the faces in deaf participants. Taken together, these results suggest that the use of lipreading and attention toward facial expression does affect profoundly the gazing behavior on faces for deaf participants, and extends toward non-communication situations with static and neutral faces.

This study suggests that early auditory deprivation and/or expertise with sign language affect the processing of faces, by altering hemispheric lateralization and modifying visual attention taken to static faces. These results emphasize the need of more detailed investigations about face perception in early deaf people and the relation between hemispheric lateralization and gazing behavior, as well as the relative influences of auditory deprivation and the use of sign language in this plasticity for face processing.

The experiment was approved by the local ethics committee (“Comité d’éthique des centre d’investigation clinique de l’inter-région Rhône-Alpes-Auvergne”, no. 2014-A00088-39). Subjects signed informed consent before participating in the experiments.

Designed the experiments: MD, OP, and DM. Performed the experiments: MD. Analyzed data: MD and DM. Wrote the manuscript: MD, DM, and OP.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.