The Neurobiology of Reading Differs for Deaf and Hearing Adults Karen Emmorey Please cite as: Emmorey, K. (2020). The neurobiology of reading differs for deaf and hearing adults. In M. Marschark and H. Knoors (Eds). Oxford Handbook of Deaf Studies in Learning and Cognition, pp. 347–359, Oxford University Press. Running head: The neurobiology of reading Karen Emmorey Laboratory for Language and Cognitive Neuroscience 6495 Alvarado Road, Suite 200 San Diego, CA 92120 USA [email protected] Acknowledgements This work was supported by a grant from the National Institutes of Health (DC014246) and grants from the National Science Foundation (BCS-1651372; BCS-1756403). The neurobiology of reading 2 Abstract Recent neuroimaging and electrophysiological evidence reveal how the reading system successfully adapts when phonological codes are relatively coarse-grained due to reduced auditory input during development. New evidence suggests that the optimal end-state for the reading system may differ for deaf versus hearing adults and indicates that certain neural patterns that are maladaptive for hearing readers may be beneficial for deaf readers. This chapter focuses on deaf adults who are signers and have achieved reading success. Although the left-hemisphere dominant reading circuit is largely similar, skilled deaf readers exhibit a more bilateral neural response to written words and sentences compared to their hearing peers, as measured by event- related potentials and functional magnetic resonance imaging. Skilled deaf readers may also rely more on neural regions involved in semantic processing compared to hearing readers. Overall, emerging evidence indicates that the neural markers for reading skill may differ for deaf and hearing adults. Keywords: deaf, reading, visual word recognition, sentence reading, fMRI, ERP The neurobiology of reading 3 Reading is a complex visual and linguistic process that differs for deaf and hearing adults because of their distinct sensory and language experiences. Changes in visual processing that stem from a lack of auditory input during development and imprecise phonological representations that result from reduced access to auditory speech can both alter the nature of the reading process. Although a great deal is known about the neural circuitry that supports reading in typical hearing adults (e.g., Dehaene, 2009; Pugh et al., 2001), much less is known about the neural regions that support skilled reading in deaf individuals. This chapter reviews our current understanding of the neurocognitive underpinnings of reading skill in deaf adults who grew up with a sign language (i.e., exposed to a sign language in early childhood). The review focuses primarily on deaf adult signers because a) they are less likely to have experienced language deprivation during childhood (e.g., Humphries et al., 2012; Glickman & Hall, 2018), which may have distinct effects on reading acquisition and b) they are less likely to access phonological codes when reading compared to deaf adults who acquired only a spoken language (e.g., Hirshorn et al., 2015; Koo, Kelly, LaSasso, & Eden, 2008). Thus, deaf signers may be more likely to exhibit neural plasticity within the reading system and may achieve reading success through alternative pathways compared to hearing speakers. All neurobiological theories of reading must specify the neurocognitive processes involved in comprehending the elemental units of written language: visually encountered words. Thus, this review first examines how the brain recognizes individual words and the factors that influence the brain’s response to printed words in deaf compared to hearing readers. The second (shorter) section of this review describes the few neuroimaging and neurophysiological studies that have investigated the processes involved in sentence-level reading in deaf compared to The neurobiology of reading 4 hearing adults. The final section concludes with a summary and suggestions for future research directions. <1> Visual Word Recognition Word reading in the hearing population is supported by a distributed neural circuitry associated with specific component processes (i.e., phonology, orthography, and semantics). Briefly, skilled word reading in hearing individuals involves a left-hemisphere dominant system comprised of temporal-parietal cortex which maps visually printed words onto phonological representations (and also binds phonological information to semantic representations), ventral inferior temporal cortex which maps visual features onto orthographic representations and includes the Visual Word Form Area, and the inferior frontal cortex which is involved in both semantic and phonological processing of written words (for review see Dehaene, 2009). Figure 1 provides a schematic illustration of these brain regions. Figure 1. Schematic of the reading circuit in the left hemisphere. The neurobiology of reading 5 In addition, much is known about the neural dynamics of word reading in the hearing population as revealed by event-related potentials (ERPs). Specifically, many studies using the visual masked priming paradigm have identified a cascade of ERP components that a) identify low-level visual features of letters (the N/P150), b) process sublexical orthographic and phonological representations (the N250), and c) process whole-word representations (the N400) (see Grainger & Holcomb, 2009, for review). In visual masked priming, orthographic, phonological, or semantic information from a briefly presented masked prime is integrated with information extracted from the target word, and the prime and target are processed as a single perceptual event – readers are unaware of seeing the prime word. Thus, priming is not subject to strategic effects, and manipulating the type of priming (e.g., phonological, orthographic, or semantic) reveals the linguistic sensitivity of various ERP components. The N170 is another ERP component that has been studied extensively in hearing readers and that is elicited by single written words (not masked). The N170 is left-lateralized in hearing adults (i.e., larger over the left hemisphere) and appears to index fine-tuning of orthographic representations as the N170 amplitude is larger to words than to other visual stimuli, such as symbol strings (e.g., Rossion, Joyce, Cottrell, & Tarr, 2003; Maurer, Brandeis, & McCandliss, 2005). In this section, recent neuroimaging and electrophysiological studies of word reading are reviewed that examine how the brain processes written words in deaf adults and whether these processes differ from hearing readers. <2> The Visual Word Form Area The visual word form area (VWFA) is located along the underside (ventral location) of the inferior temporal cortex (see Figure 1). This region preferentially responds to written words and The neurobiology of reading 6 encodes abstract orthographic representations (e.g., the neural response is insensitive to case, font, or script; see Dehaene & Cohen, 2011, for review). As hearing children learn to read, this region becomes tuned to print, with better readers exhibiting stronger activation. Adults who are illiterate do not show increased neural activity in the VWFA when viewing written words compared to similar non-word visual stimuli, but VWFA activation increases with increased literacy. Thus far, most studies have found no difference in VWFA activation between deaf and hearing readers (Aparicio, Gounot, Demont, & Metz-Lutz, 2007; Emmorey, Weisberg, McCullough, & Petrich, 2013; Waters et al., 2007; Wang, Caramazza, Peele, Han, & Bi, 2015). The location and extent of activation within the VWFA when recognizing visual words is similar for both groups, but how this region connects to other brain areas differs. Wang et al. (2015) found that the functional connectivity between the VWFA and auditory speech areas in left superior temporal cortex was reduced for congenitally deaf readers, but the connectivity between the VWFA and the frontal and parietal regions of the reading circuit was similar for deaf and hearing readers. The authors concluded that auditory speech experience does not significantly alter the location or response strength of the VWFA. However, there are mixed results with respect to whether reading skill impacts neural activity within the VWFA for deaf adults. Corina, Lawyer, Hauser, and Hirshorn (2013) found greater activation for more proficient deaf readers, while Emmorey, McCullough, and Weisberg (2016) found no difference between skilled and less-skilled deaf readers in this region. Studies that compared deaf readers with more skilled hearing readers have also reported no group differences in activation in this region (Aparicio et al., 2007; Wang et al., 2015; Waters et al., 2007). These latter findings suggest that a primary marker of poor reading in hearing individuals, The neurobiology of reading 7 namely reduced activation in the VWFA (e.g., Hoeft et al., 2007), may not constitute an indicator of reading skill for deaf individuals. Rather, Emmorey et al. (2016) found that better reading ability in deaf adults was associated with increased neural activation in a region that was in front of (anterior to) the VWFA, when deaf readers made a semantic decision about words. Emmorey et al. speculated that this region may be involved in mapping orthographic word-level representations onto semantic representations (e.g., Purcell, Shea, & Rapp, 2014) and that better deaf readers may have stronger or more finely-tuned links between orthographic and semantic lexical representations.