Visual habituation in deaf and hearing infants

RESEARCH ARTICLE Visual habituation in deaf and hearing infants Claire Monroy ID1,2☯*, Carissa Shafto3☯, Irina Castellanos1,2, Tonya Bergeson4, Derek Houston1,2 1 Department of Otolaryngology—Head and Neck Surgery, Ohio State University Wexner Medical Center, Columbus, Ohio, United States of America, 2 Nationwide Children’s Hospital, Columbus, Ohio, United States of America, 3 Insight Data Science, New York City, New York, United States of America, 4 Department of Communication Sciences and Disorders, Butler University, Indianapolis, Indiana, United States of America ☯ These authors contributed equally to this work. * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Monroy C, Shafto C, Castellanos I, Bergeson T, Houston D (2019) Visual habituation in deaf and hearing infants. PLoS ONE 14(2): e0209265. https://doi.org/10.1371/journal. pone.0209265 Editor: Jordy Kaufman, Swinburne University of Technology, AUSTRALIA Received: May 14, 2018 Accepted: December 3, 2018 Published: February 6, 2019 Copyright: © 2019 Monroy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This research was supported by grants from the NIDCD (https://www.nidcd.nih.gov/) to C. L.S. (F31 DC010281) and D.M.H. (R01 DC006235). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abstract Early cognitive development relies on the sensory experiences that infants acquire as they explore their environment. Atypical experience in one sensory modality from birth may result in fundamental differences in general cognitive abilities. The primary aim of the current study was to compare visual habituation in infants with profound hearing loss, prior to receiving cochlear implants (CIs), and age-matched peers with typical hearing. Two complementary measures of cognitive function and attention maintenance were assessed: the length of time to habituate to a visual stimulus, and look-away rate during habituation. Findings revealed that deaf infants were slower to habituate to a visual stimulus and demonstrated a lower look-away rate than hearing infants. For deaf infants, habituation measures correlated with language outcomes on standardized assessments before cochlear implantation. These findings are consistent with prior evidence suggesting that habituation and look-away rates reflect efficiency of information processing and may suggest that deaf infants take longer to process visual stimuli relative to the hearing infants. Taken together, these findings are consistent with the hypothesis that hearing loss early in infancy influences aspects of general cognitive functioning. Introduction Infants learn about the world through their multimodal interactions with objects and other people in their environment [1–3]. The atypical functioning of one sensory system may result in widespread effects across multiple sensory modalities and cognitive domains [4,5]. The auditory system, in particular, is thought to play a pivotal role in shaping the cognitive system [6]. As a result, researchers have recently begun to investigate the impact of prelingual hearing loss on cognition from a developmental perspective [7,8]. Several studies have shown that deaf children exhibit poorer performance in multiple nonverbal cognitive skills compared to their hearing peers. These include visual controlled attention (e.g., [9]), sequence processing [10,11], and working memory [12]. Other studies have also reported differences in motor abilities that require cognitive skills, such as in spatial coordination [13] and visual-motor integration skills [14]. Together, these findings suggest that PLOS ONE | https://doi.org/10.1371/journal.pone.0209265 February 6, 2019 1 / 15 Hearing loss and visual habituation general cognitive abilities differ between deaf and hearing children. However, the underlying sources of these differences are still unknown, as is when the differences emerge during infancy. Differences between deaf and hearing individuals may initially arise from cortical crossmodal re-organization. In the absence of sound input, the auditory cortex responds to visual and somatosensory input [7,15,16]. Visual cross-modal re-organization has also been demonstrated in children as young as five years of age [17]. Cross-modal plasticity is thought to arise via compensatory mechanisms of the remaining senses following a sensory loss. However, evidence for poorer performance in deaf individuals has contributed to sensory deprivation hypotheses, which stem from the assumption that our sensory systems are intrinsically multimodal [1]. Atypical functioning in one modality will therefore have cascading consequences throughout other sensory modalities. Given the evidence that multimodal sensory processing underlies cognition (e.g., embodied cognition theories), atypical sensory functioning should also affect cognitive abilities. One example, proposed by Smith and colleagues [18], is the hypothesis that hearing loss causes poorer multimodal sensory integration, which, in turn, causes deficits in visual selective attention and cognitive control. These authors suggest that multisensory integration is essential for the development of attentional skills in each individual sensory modality. In support of this hypothesis, they report data showing that cognitive control and visual selective attention in deaf children improves following cochlear implantation [18]. Another example of a sensory deprivation hypothesis is the auditory scaffolding hypothesis, which emphasizes the importance of auditory input for typical development of cognitive functions [19]. According to this hypothesis, sound provides experience with naturally sequential input that is vital for developing general sequence learning abilities. Sequence learning, in turn, influences a variety of other domain-general cognitive abilities and can have widespread consequences on multiple aspects of development. An alternate explanation is that deaf children’s performance on cognitive and attentional tasks differs from that of hearing children because of their limited language experiences, rather than general cognitive abilities [20–22]. Early language and communicative experiences are critical for the typical development of social and cognitive skills [23]. However, the majority of deaf infants experience mismatched communication exchanges with their hearing parents— that is, the reciprocal communication pattern in typical parent-infant interactions is disrupted when the infant’s hearing status does n (...truncated)