Human peripheral visual perception is affected by sensory, developmental, and environmental experience. The visual system has inherent plasticity, peripheral vision in particular showing a high capacity for plasticity and the potential for peripheral visual plasticity has been previously underestimated (Burnat, 2015). Both the peripheral retina and the magnocellular visual pathway have emergent, immature topographies that may facilitate high levels of visual plasticity throughout life. Far peripheral vision plays a crucial role in monitoring the environment, especially in the absence of sound.

Several visual changes have been noted in association with deafness. Bosworth and Dobkins (2002) showed that deaf adults performed significantly better to peripheral, but not central visual stimuli. Proksch and Bavelier (2002) used a visual search paradigm to report that deaf individuals had greater visual attentional resources in the visual periphery, and less in central vision. Neville and Lawson (1987a,b) found enhanced attention to the visual periphery in a motion decision task, coordinated with event-related potential (ERP) responses from the occipital cortex of deaf participants to peripheral stimuli. Bavelier et al. (2001) by means of fMRI, detected greater recruitment of the motion selective area V5/MT for deaf participants when they attended peripherally rather than centrally. Fine et al. (2005) found that fMRI responses to visual stimuli were uniquely represented in the auditory cortex of deaf participants, and this effect was not seen in adult participants who were children of deaf adults (CODAs), signing from birth. Bavelier et al. (2006) summarized that not all aspects of vision are improved in deaf individuals—deaf adults showing slower reactions in central visual cognitive tasks (Proksch and Bavelier, 2002). Bavelier et al. (2006) argue that selective visual changes occur which compensate for those aspects of vision that would normally benefit from the combined auditory and visual inputs. In line with this, Codina et al. (2011b) found altered retinal ganglion cell layer distribution to support peripheral vision, and increased retinal ganglion cell number and structural changes correlated with increased peripheral vision performance. Deafness therefore has a differential influence on both the structure and behavior of the remaining senses such as vision.

It is not only deafness that has been shown to promote a peripheral visual advantage in humans. Habitual playing of computer games has been linked with improved localization of a peripheral target amongst distractors (Green and Bavelier, 2003), and increased visual field (VF) area Buckley et al. (2010). Memmert et al. (2009) found specific visual attention improvements between athletes and non-athletes when the stimuli were most similar to their practiced sport. Muiños and Ballesteros (2013) reported that karate athletes were faster at localizing peripheral visual stimuli than non-athletes. They suggested that the rapidity of response in their athletes may be due to the suddenly appearing, peripherally attended, opponent maneuver. Different patterns of visual skills may result in specifically trained motor responses to peripheral visual stimuli. There is consensus amongst several authors that the visual differences found between athletes and non-athletes are not in the “hardware” of functional visual pathway changes, but in the “software,” using perception and visual-cognitive processes more efficiently, employing skill utilizing strategies made effective with practice (Abernethy et al., 1994; Muiños and Ballesteros, 2013). Schubert et al. (2015) conducted a detailed investigation on the training effects of video gaming on visual attention. They found that video gamers showed increased visual processing speeds in the lower aspects of the VF. The video gamers did not change their attention allocation strategy, with high speed processing demonstrated in all display locations. However, the video gaming advantage was seen specifically in areas where non-experts performed less well, with higher speed visual processing and shorter minimal exposure duration needed to begin perceptual processing. These higher processing speeds in response to training might improve the temporal resolution of attention and allow attention to be moved between focally and peripherally presented stimuli.

What is particularly interesting about deaf individuals is that the altered sensory experience of deafness clearly brings about unique sensory and cognitive changes. However, most deaf persons are also immersed, to some degree, in a visual spatial language such as British Sign Language (BSL), which in itself places altered conceptual and sensory demands on the visual system, quite different to spoken language (see Bavelier et al., 2006 for a review).

During signed language conversation, fluent, signing individuals typically focus on the face of the person signing to them (Siple et al., 1978; Muir and Richardson, 2005; Agrafiotis et al., 2006). Taking the visuospatial nature of signed language into account, signed language is therefore likely to stimulate peripheral vision in a manner extraordinary to spoken language. Indeed, Swisher et al. (1989) demonstrated that deaf adults could understand American Sign Language (ASL) signs using peripheral vision only, between 45° and 61° eccentric to fixation, whereas hearing individuals could not identify large words presented at similar eccentricities. In signed language space is used both topographically and referentially (MacSweeney et al., 2008). Signing space extends from the navel to above the head and “neutral space” is the area in front of the signer's body at mid-lower chest level one where most of the BSL signs occur (British Deaf Association, 1992). The majority of “words” in ASL are produced below eye level (Teuber et al., 1980); therefore, it may be that the inferior field of vision is particularly stimulated by signed language experience.

Familiarization with visuospatial language does not seem to produce the same enhancements in peripheral vision as revealed in deaf adults: the visual advantages cited earlier in deaf individuals have not been found in hearing signing populations (Neville and Lawson, 1987a,b; Bosworth and Dobkins, 2002; Proksch and Bavelier, 2002; Fine et al., 2005). However, these experiments did not test as far in the periphery as we have tested here. Nevertheless, signing has produced distinct cortical and visual changes. Cortical adaptations have been observed in both hearing and deaf signers in response to language perception. Although a right hemisphere predilection and therefore left VF advantage is widely accepted in the general population (Paillard et al., 1981; Paillard and Amblard, 1985; Clarke et al., 2000), Bosworth and Dobkins (1999, 2002) demonstrated a left hemisphere lateralization and right VF advantage for motion processing in signers, whether deaf or hearing. Bavelier et al. (2001) found early exposure to ASL led to greater reliance on the left hemisphere motion selective area V5/MT. The left, language dominant hemisphere may become increasingly activated by motion processing in deaf and hearing signers, leading to a right VF advantage for the processing of visual motion (Neville and Lawson, 1987a; Bosworth and Dobkins, 1999; Bavelier et al., 2001). Cardin et al. (2013) in an fMRI study of distinct deaf signers and deaf lip readers showed that cortical regions adjust to process the different signals—either speech reading or signed language and that functionally distinct cortical substrates separate deaf adults who sign from those who speech read.

Given the plasticity of the visual periphery to maximize its response to the pattern of visual skills required, one might expect BSL experience itself to influence far peripheral vision and RTs therein. In a previous paper (Codina et al., 2011a) in which we reported deaf and hearing children's peripheral visual performance development on a far peripheral vision task (30–85°), young deaf children (aged 5–8 years) were initially slower to respond to peripheral stimuli than hearing children, they performed similarly at ages 9–11 years, and were significantly faster than controls at ages 12–15 years. To the authors' knowledge, the RT advantage consistently observed in deaf adults has not been thoroughly investigated across the far peripheral field and neither has it been investigated in hearing sign language users. The aim of the current study was to investigate far peripheral visual sensitivity and RT in early onset deaf adults and BSL interpreters, to explore the different and separable effects of auditory deprivation and experience with a visuospatial language.

Deaf participants reacted significantly faster to the peripherally presented stimuli when compared to the hearing group and BSL interpreter group. This pattern of results was found across all VF locations and up to the maximum eccentricities tested. Faster RTs in early onset deaf adults found in this study are consistent with the faster deaf RTs reported in the literature (Parasnis and Samar, 1985; Neville and Lawson, 1987a; Loke and Song, 1991; Stivalet et al., 1998; Bosworth and Dobkins, 2002; Proksch and Bavelier, 2002). Importantly, however, the current study demonstrates a greater advantage in the far peripheral VF, in a range of peripheral vision (30–85°), which has not previously been investigated. Peripheral visual acuity is increasingly poor at increasing eccentricities, thereby sound confers the greatest advantage at this range of eccentricities. At far peripheral locations our study finds markedly speeded RTs in deaf participants as well as moderately speeded RTs in full time BSL interpreters.

The fastest RTs for all groups and the fastest RTs overall were displayed by the deaf group in inferior and temporal aspects of the VF. One might expect the greatest advantage for deaf individuals in these VF areas where the majority of “words” in signed language would occur (Teuber et al., 1980). However, the significantly speeded RTs were identifiable in all meridian locations and could not be localized to any particular region of the VF. The deaf RT advantage was not significant at all eccentricities, likely because of the increased standard error in eccentricity data. The significant differences in all Figure 4 post-hoc analyses revealed differences only between deaf and hearing groups and not between BSL and hearing or between BSL and deaf groups. This deaf advantage at these far eccentricities is consistent with Swisher et al.'s (1989) finding that deaf adults could reliably identify ASL signs 45° and 61° eccentric to fixation using peripheral vision only and with Buckley et al. (2010) report of significantly larger VFs in deaf adults, using kinetic stimuli at a similar range of eccentricities. Buckley and colleagues found that the areas of most significant increase were the inferior and temporal aspects of the VF—regions most stimulated by signed language but also the most expansible aspects of the VF. In deaf adults the RT advantage results from the combined effects of auditory deprivation and the cross-modal plasticity evidenced to this (Fine et al., 2005), as well as immersion into an entirely visual language. However, our results suggest that visuo-spatial BSL language immersion alone does not confer the same peripheral vision RT advantage that auditory deprivation does.

The visuo-cognitive influences of auditory deprivation and signed language exposure are likely to be distinct, yet segregating one from the other is difficult. As previously described, 11 of our deaf group reported BSL as their native language, yet analyses by native language showed no significant influence of native language on RT. However, even in the minority of predominantly aural deaf individuals (for example those married to hearing persons) cumulative exposure to sign language throughout life is still significant. Cardin et al. (2013) reported that after plastic reorganization in deafness, cortical regions adapt to process the different types of signal—either lip reading or signed language—and that functionally distinguishable substrates are present at the cortical level between deaf who sign and deaf who lip read.

Interestingly, Emmorey et al. (2009) found an eye gaze fixation pattern difference between beginning and native signers: beginning signers fixated nearer to the signer's mouth so to perceive lip mouthings more clearly; whereas fluent signers fixated nearer to the interlocutor's eyes. Thus increased experience with signed language was related to a greater ability to perceive signed and mouthed information more peripherally. In our data, the hearing signers were all currently working BSL interpreters, having been fluent in BSL for a minimum of 6 years. They might have therefore adapted during the course of their BSL careers to move further away from lower face fixation as peripheral vision adapts to improve sensitivity to the most peripheral areas most utilized by signed language and facial expression.

In a previous paper (Codina et al., 2011b), we reported that the retinal nerve fiber layer in the eyes of early onset deaf adults was differentially distributed to support peripheral vision, particularly temporal aspects of the VF where the left and right VFs do not overlap and neural resources may be most influential. Fine et al. (2005) reported that the cross-modal plasticity within the auditory cortex responding to signed language was not present in either non-profoundly deaf individuals nor present in hearing signers. The results showing that facilitating this level of neural reorganization requires a dramatically altered sensory experience. That said, it is perhaps only in profoundly deaf adults that increased neural circuitry to the remaining senses is expected, consistent with Fine et al. (2005) and Codina et al. (2011b), which might facilitate the RT decrease identified in the far periphery in this study. However, electrophysiological (Osorio et al., 2010) and brain imaging studies (Ballesteros et al., 2013) have found altered neural correlates in response to simple behavioral training in conceptual object priming, and this in itself may be evidence of compensatory neural activity. Our results are comparable with Buckley et al. (2010) where habitual video game players showed enhanced areas of peripheral visual sensitivity in comparison to non-video-game players, which were even larger in early onset deaf adults. This suggests that enhancement of peripheral vision may be partially mediated by visual attention, with additional compensatory improvement due to sensory deprivation.

Based on our previous research, it is likely that the reduced RTs identified in deaf adults were slow to develop (Codina et al., 2011a), and were perhaps facilitated by altered neural substrates and compensatory neural activity (Codina et al., 2011b). It is possible that similar neural changes may have occurred in hearing signers as well, although this has not yet been tested. However, the visual differences found between hearing signers and non-signers might be similar to the differences found between athletes and non-athletes, not so much in the “hardware” of functional visual pathway changes, but in the “software” efficiency of perceptive and attentional processes (Abernethy et al., 1994; Muiños and Ballesteros, 2013).

Recruitment of BSL interpreters was particularly difficult due to the national shortage of BSL interpreters at the present time (McAleer, 2006), and as a consequence, the mean age of the BSL interpreter group is slightly higher than for deaf and hearing groups. However, simple RT is known to increase with age (Der and Deary, 2006) and become more variable (Hultsch et al., 2002). Also of note was that none of the BSL interpreter group played computer games, as computer game playing has been shown to improve peripheral vision (Green and Bavelier, 2003; Buckley et al., 2010). Therefore, to find faster RTs in this slightly older and non-computer game playing group is a more striking result.

The RTs we report in our study are larger than those studies employing standard kinetic perimetry (Grobbel et al., 2016). Grobel and colleagues, with varying ages of adult participants, reported RTs of 391—522ms. However, theirs was a motion detection task, more suited to the peripheral visual pathway and required the simple press of a button, whereas our experiment utilized static eccentric stimuli and an 8-alternative forced choice task and was therefore conceptually more demanding.

All groups showed a slight left VF RT advantage, in line with the right hemisphere predilection for visual-spatial activity, widely reported in the literature (Paillard et al., 1981; Paillard and Amblard, 1985; Clarke et al., 2000) and reported in hearing non-signers by Bosworth and Dobkins (1999, 2002), Neville and Lawson (1987b). In a stochastic motion task within 15° of fixation, Bosworth and Dobkins (2002) reported that both deaf and hearing signers displayed the opposite pattern of results to hearing non-signers, finding a right VF RT advantage in deaf and hearing signers. We did not find this right VF advantage in the far periphery tested in our study. However, the significant RT reduction in the deaf group's right VF, in comparison with hearing controls, and the highly similar right and left VF RTs in our deaf group may indicate a sensory compensatory mechanism to advance the typical left RT advantage additionally to the right VF. Therefore, auditory deprivation rather than BSL exposure seems to influence the right VF RT. This is interesting in that lesion and neuroimaging studies have consistently reported that the neurobiology of signed language is very similar to spoken language, principally recruiting the left lateralized perisylvian network no matter which language is involved (MacSweeney et al., 2008).

In light of the markedly reduced RTs for the deaf group it is interesting to consider which particular aspects of visuomotor processing may be enhanced by auditory deprivation and training. Auditory deprivation may speed peripheral perception by use of compensatory cortical plasticity and exposure to a language stimulating the visual periphery may call into play alternative visual attention allocation strategies which may, in turn speed the visuomotor response. When considering the visuomotor nature of this study's task it is of note that the deaf group contained a high number of left handed individuals and this finding is consistent with other studies (Papadatou-Pastou and Sáfár, 2016). Atypical handedness may contribute to VF laterality differences, though had no significant effect on our results. Bavelier et al. (2006) put forward four hypotheses in relation to deaf neural and attentional adaptations. They proposed that adaptation may be genetic; that areas V1 and V2 may be more susceptible to intramodal recruitment to visual attention; that multisensory associative cortical areas might reorganize to the remaining modalities such as vision; or that auditory cortex might reorganize to mediate other functions such as vision. Our results suggest that the most speeded responses, highlighting the highest visual attention in the far periphery in deaf adults, supersede the increased visual attention brought about by practice with a visual-spatial language alone, signifying different mechanisms of visual compensation.

Deaf adults demonstrated significantly faster RTs than both hearing non-signers and hearing BSL interpreters to a range of far peripheral briefly presented static stimuli and this advantage was consistent across all VF locations up to 85° eccentric to fixation. BSL interpreters displayed faster RTs than hearing non-signing adults across the entire VF. Early onset deafness leads to visual compensation in the form of much faster peripheral vision RTs consistent with the cross-modal plasticity benefits to vision of auditory deprivation and use of a visual spatial language. The deaf RT advantage is most apparent in the right VF, where hearing responses are significantly slower. Fluency in BSL without deafness also leads to rapid responses to peripheral stimuli, although not to the same degree as deafness. Daily immersion in a visual-spatial language benefits visual responsiveness to stimuli in the peripheral VF.

Ethical approval was granted by the University of Sheffield, Department of Psychology, Ethics Committee. Participants were invited by the experimenter by letter, email or by personal invitation to take part. The researcher gave every participant a participant information sheet that had been given ethical approval. This information was additionally given to the deaf participants in British Sign Language as required. Participants gave full written, informed consent before taking part in the experiment. Deaf adults were given the information verbally, in writing and in British Sign Language as each preferred. Participants were fully informed of the procedure in the language of their choosing. Participants all knew the test procedure and had the opportunity to ask questions under conditions of full lighting before any testing began.

DB, OP, and CC designed the test equipment, were involved in piloting and refining the experiment and in the ethics process. CC collected and analyzed the data. AL and HB assisted in the interpretation of the data and further analysis. The paper was written by CC with contributions from all authors.