Cross-modal Neuroplasticity Research Articles

Neurocognitive outcomes in young adults with cochlear implants: The role of early language access and crossmodal plasticity

Many children with profound hearing loss have received cochlear implants (CI) to help restore some sense of hearing. There is, however, limited research on long-term neurocognitive outcomes in young adults who have grown up hearing through a CI. This study compared the cognitive outcomes of early-implanted (n = 20) and late-implanted (n = 21) young adult CI users, and typically hearing (TH) controls (n=56), all of whom were enrolled in college. Cognitive fluidity, nonverbal intelligence, and American Sign Language (ASL) comprehension were assessed, revealing no significant differences in cognition and nonverbal intelligence between the early and late-implanted groups. However, there was a difference in ASL comprehension, with the late-implanted group having significantly higher ASL comprehension. Although young adult CI users showed significantly lower scores in a working memory and processing speed task than TH age-matched controls, there were no significant differences in tasks involving executive function shifting, inhibitory control, and episodic memory between young adult CI and young adult TH participants. In an exploratory analysis of a subset of CI participants (n = 17) in whom we were able to examine crossmodal plasticity, we saw greater evidence of crossmodal recruitment from the visual system in late-implanted compared with early-implanted CI young adults. However, cortical visual evoked potential latency biomarkers of crossmodal plasticity were not correlated with cognitive measures or ASL comprehension. The results suggest that in the late-implanted CI users, early access to sign language may have served as a scaffold for appropriate cognitive development, while in the early-implanted group early access to oral language benefited cognitive development. Furthermore, our results suggest that the persistence of crossmodal neuroplasticity into adulthood does not necessarily impact cognitive development. In conclusion, early access to language – spoken or signed – may be important for cognitive development, with no observable effect of crossmodal plasticity on cognitive outcomes.

Gray matter density changes in children with congenital severe sensorineural deafness: a voxel-based morphometric study.

Early hearing loss could cause abnormal brain development, which has been linked to the complex process known as cross-modal neuroplasticity. However, previous studies investigating the brain structure of infants with congenital severe sensorineural hearing loss (CSSHL) are scarce and have yielded inconsistent results. This study aimed to further explore the gray matter (GM) density changes in children with CSSHL. Fifteen children aged 0-5 years with CSSHL and 11 healthy children as controls (aged 0-5 years) were recruited. Each participant underwent a structural MRI scan. The voxel-based morphometry method was performed to evaluate GM density for each participant and analyze their characteristics. It was discovered that: (1) GM density of the right superior temporal gyrus and caudate in the CSSHL group was smaller than that of healthy controls (HC). However, GM density was larger in the left posterior central gyrus, superior frontal gyrus, inferior parietal lobule and right cerebellum in the CSSHL group compared with HC. (2) The GM density value of the left superior frontal gyrus and inferior parietal lobule was negatively correlated with age. However, the GM density value of the right superior temporal gyrus in the CSSHL group was positively correlated with age. Compared with HC, the GM density of CSSHL children was larger in somatosensory areas (including left superior frontal gyrus, posterior central gyrus, inferior parietal lobule and right cerebellum), whereas GM density was smaller in auditory-related areas (such as the right superior temporal gyrus and caudate). Moreover, GM density change was influenced by the duration of hearing deprivation.

A framework to account for the effects of visual loss on human auditory abilities.

Until recently, a commonly held view was that blindness resulted in enhanced auditory abilities, underpinned by the beneficial effects of cross-modal neuroplasticity. This viewpoint has been challenged by studies showing that blindness results in poorer performance for some auditory spatial tasks. It is now clear that visual loss does not result in a general increase or decrease in all auditory abilities. Although several hypotheses have been proposed to explain why certain auditory abilities are enhanced while others are degraded, these are often limited to a specific subset of tasks. A comprehensive explanation encompassing auditory abilities assessed in fully blind and partially sighted populations and spanning spatial and non-spatial cognition has not so far been proposed. The current article proposes a framework comprising a set of nine principles that can be used to predict whether auditory abilities are enhanced or degraded. The validity of these principles is assessed by comparing their predictions with a wide range of empirical evidence concerning the effects of visual loss on spatial and non-spatial auditory abilities. Developmental findings and the effects of early- versus late-onset visual loss are discussed. Ways of improving auditory abilities for individuals with visual loss and reducing auditory spatial deficits are summarized. A new Perceptual Restructuring Hypothesis is proposed within the framework, positing that the auditory system is restructured to provide the most accurate information possible given the loss of the visual signal and utilizing available cortical resources, resulting in different auditory abilities getting better or worse according to the nine principles. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Auditory Space Perception in the Blind: Horizontal Sound Localization in Acoustically Simple and Complex Situations.

Even though it is widely believed that cross-modal neuroplasticity in blindness results in enhanced auditory spatial abilities, a growing number of studies also indicate disadvantages of blind persons for specific, more demanding audiospatial tasks. Here, the effects of blindness on horizontal sound localization were compared for simple localization of target sounds presented in isolation and target localization in an acoustically complex ( cocktail-party) situation with multiple distractor sounds. While performances of blind and sighted subjects were similar in the cocktail-party setting, a significant disadvantage of blind subjects was found for simple localization of sound sources presented in the center of the frontal space, with the mean absolute error being more than twice that of controls for targets in the median plane. The latter result could be due to the lack of visual calibration of auditory space, which may, in sighted persons, be most effective in the region of maximum visual acuity. On the other hand, the normal performance of blind persons in cocktail-party localization could be explained by the fact that this task, in addition to genuine spatial analysis, critically involved spectrotemporal analysis of the auditory scene to separate different sources for which superior performance is known from previous research.

Pattern of neural divergence in adults with prelingual deafness: Based on structural brain analysis

Sensory input for hearing plays a significant role in the development of human brain. Absence of an early auditory input leads to the alteration of important neural regions, which in turn results in a complex process known as cross-modal neuroplasticity. Previous studies related to the structural brain alteration of adult deaf individuals have shown inconsistent results. To address this issue, we investigated the brain morphology in 50 prelingual adult deaf individuals and compared it with the same number of individuals with normal hearing, using structural magnetic resonance imaging and three inter-related but completely distinct analysis methods namely univariate approach (voxel based morphometry), multivariate approach (source based morphometry), and projection based cortical thickness. The findings from all these inter-related analyses suggest alterations in important neural regions such as bilateral superior temporal gyrus, bilateral inferior temporal, bilateral fusiform gyrus, and bilateral middle frontal. These findings also justify a strong ventral visual pathway in the deaf group. We suggest that these morphological alterations in important brain regions are due to the compensatory cross-modal reorganization.

Atypical white-matter microstructure in congenitally deaf adults: A region of interest and tractography study using diffusion-tensor imaging

Considerable research documents the cross-modal reorganization of auditory cortices as a consequence of congenital deafness, with remapped functions that include visual and somatosensory processing of both linguistic and nonlinguistic information. Structural changes accompany this cross-modal neuroplasticity, but precisely which specific structural changes accompany congenital and early deafness and whether there are group differences in hemispheric asymmetries remain to be established. Here, we used diffusion tensor imaging (DTI) to examine microstructural white matter changes accompanying cross-modal reorganization in 23 deaf adults who were genetically, profoundly, and congenitally deaf, having learned sign language from infancy with 26 hearing controls who participated in our previous fMRI studies of cross-modal neuroplasticity. In contrast to prior literature using a whole-brain approach, we introduce a semiautomatic method for demarcating auditory regions in which regions of interest (ROIs) are defined on the normalized white matter skeleton for all participants, projected into each participants native space, and manually constrained to anatomical boundaries. White-matter ROIs were left and right Heschl's gyrus (HG), left and right anterior superior temporal gyrus (aSTG), left and right posterior superior temporal gyrus (pSTG), as well as one tractography-defined region in the splenium of the corpus callosum connecting homologous left and right superior temporal regions (pCC). Within these regions, we measured fractional anisotropy (FA), radial diffusivity (RD), axial diffusivity (AD), and white-matter volume. Congenitally deaf adults had reduced FA and volume in white matter structures underlying bilateral HG, aSTG, pSTG, and reduced FA in pCC. In HG and pCC, this reduction in FA corresponded with increased RD, but differences in aSTG and pSTG could not be localized to alterations in RD or AD. Direct statistical tests of hemispheric asymmetries in these differences indicated the most prominent effects in pSTG, where the largest differences between groups occurred in the right hemisphere. Other regions did not show significant hemispheric asymmetries in group differences. Taken together, these results indicate that atypical white matter microstructure and reduced volume underlies regions of superior temporal primary and association auditory cortex and introduce a robust method for quantifying volumetric and white matter microstructural differences that can be applied to future studies of special populations.

Brain Plasticity in Blind Subjects Centralizes Beyond the Modal Cortices.

It is well established that the human brain reorganizes following sensory deprivations. In blind individuals, visual processing regions including the lateral occipital cortex (LOC) are activated by auditory and tactile stimuli as demonstrated by neurophysiological and neuroimaging investigations. The mechanisms for such plasticity remain unclear, but shifts in connectivity across existing neural networks appear to play a critical role. The majority of research efforts to date have focused on neuroplastic changes within visual unimodal regions, however we hypothesized that neuroplastic alterations may also occur in brain networks beyond the visual cortices including involvement of multimodal integration regions and heteromodal cortices. In this study, two recently developed graph-theory based functional connectivity analyses, interconnector analyses and local and distant connectivity, were applied to investigate functional reorganization in regional and distributed neural-systems in late-onset blind (LB) and congenitally blind (CB) cohorts each compared to their own group of sighted controls. While functional network alterations as measured by the degree of differential links (DDL) occurred in sensory cortices, neuroplastic changes were most prominent within multimodal and association cortices. Subjects with LB showed enhanced multimodal integration connections in the parieto-opercular, temporoparietal junction (TPJ) and ventral premotor (vPM) regions, while CB individuals exhibited increased superior parietal cortex (SPC) connections. This study reveals the critical role of recipient multi-sensory integration areas in network reorganization and cross-modal plasticity in blind individuals. These findings suggest that aspects of cross-modal neuroplasticity and adaptive sensory-motor and auditory functions may potentially occur through reorganization in multimodal integration regions.

FMRI correlates of different components of Braille reading by the blind

Brain activations in early-blind subjects during Braille reading indicate considerable cross-modal neuroplasticity in posterior brain areas. Up to now it is, however, not clear how far such neuroplastic reorganization processes reach and whether a specific brain activation pattern corresponds to a specific component of the Braille reading task. Therefore, this fMRI study investigates whether different cortical areas are functionally specialized for different aspects of Braille reading. The comprehensive Braille reading task was contrasted to three control tasks representing subcomponents of Braille reading (passive tactile stimulation, active tactile pattern recognition, Braille imagery). Results in 14 early-blind subjects indicate that only occipital and basal temporo-occipital brain areas show specific fMRI correlates for Braille reading. Central rolandic brain activations correlated with basic somatosensory processing and superior temporal activations were associated with higher level stimulus-independent language processing. In these latter areas no indications for neuroplastic reorganizations specific for Braille reading were found, despite strong activations during the Braille reading task.

Neural plasticity of voice processing: Evidence from event-related potentials in late-onset blind and sighted individuals.

Intra- and crossmodal neuroplasticity have been reported to underlie superior voice processing skills in congenitally blind individuals. The present study used event-related potentials (ERPs) in order to test if such compensatory plasticity is limited to the developing brain. Late blind individuals were compared to sighted controls in their ability to identify human voices. A priming paradigm was employed in which two successive voices (S1, S2) of the same (person-congruent) or different speakers (person-incongruent) were presented. Participants made an old-young decision on the S2. In both groups ERPs to the auditory S2 were more negative in person-incongruent than in person-congruent trials between 200-300 ms. A topographic analysis suggested a more posteriorly shifted distribution of the Person Match effect (person-incongruent minus person-congruent trials) in late blind individuals compared to sighted controls. In contrast to congenitally blind individuals, late blind individuals did not show an early Person Match effect in the time range of the N1, suggesting that crossmodal compensation is mediated by later processing steps rather than by changes at early perceptual levels.

Use of sensory substitution devices as a model system for investigating cross-modal neuroplasticity in humans.

Blindness provides an unparalleled opportunity to study plasticity of the nervous system in humans. Seminal work in this area examined the often dramatic modifications to the visual cortex that result when visual input is completely absent from birth or very early in life (Kupers and Ptito, 2014). More recent studies explored what happens to the visual pathways in the context of acquired blindness. This is particularly relevant as the majority of diseases that cause vision loss occur in the elderly. Our lab and others have demonstrated compromised visual pathway integrity in those with peri-natal and acquired blindness (Schoth et al., 2006; Chan et al., 2012; Li et al., 2013; Lee et al., 2014; Dietrich et al., 2015; Ho et al., 2015; Reislev et al., 2015). Additional studies have begun to examine the changes occurring with certain disease states: patients suffering from retinitis pigmentosa, optic neuritis, and glaucoma, all so far demonstrate deterioration of the white matter tract architecture as a function of disease severity (Garaci et al., 2009; Gabilondo et al., 2014; Ohno et al., 2015). This evidence indicates that the visual system as a whole is profoundly susceptible to degeneration even with small amounts of vision loss. On the surface, these investigations appear to have negative implications for vision restoration efforts. Yet, parallel studies which examine the phenomenon of cross-modal plasticity suggest that a remodeling of the central nervous system is possible, such that areas of the brain which have been deprived of normal afferent input are able to reconstitute themselves to be receptive to alternative sensory channels (Merabet and Pascual-Leone, 2010; Kupers and Ptito, 2014). The literature includes several examples of investigations which show that the visual cortex will react to tactile and auditory stimuli in the blind but will be less readily recruited in sighted patients (Merabet and Pascual-Leone, 2010). Moreover, cross-modal interactions have been demonstrated well beyond the traditional “critical period” and into late adulthood, albeit perhaps in a less robust fashion (Sadato et al., 2002; Bedny et al., 2012; Collignon et al., 2013). The notion that the adult brain is still capable of significant structural and functional remodeling after vision loss provides opportunities to restore vision through mechanical or biological means.

Neural correlates associated with superior tactile symmetry perception in the early blind

Symmetry is an organizational principle that is ubiquitous throughout the visual world. However, this property can also be detected through non-visual modalities such as touch. The role of prior visual experience on detecting tactile patterns containing symmetry remains unclear. We compared the behavioral performance of early blind and sighted (blindfolded) controls on a tactile symmetry detection task. The tactile patterns used were similar in design and complexity as in previous visual perceptual studies. The neural correlates associated with this behavioral task were identified with functional magnetic resonance imaging (fMRI). In line with growing evidence demonstrating enhanced tactile processing abilities in the blind, we found that early blind individuals showed significantly superior performance in detecting tactile symmetric patterns compared to sighted controls. Furthermore, comparing patterns of activation between these two groups identified common areas of activation (e.g. superior parietal cortex) but key differences also emerged. In particular, tactile symmetry detection in the early blind was also associated with activation that included peri-calcarine cortex, lateral occipital (LO), and middle temporal (MT) cortex, as well as inferior temporal and fusiform cortex. These results contribute to the growing evidence supporting superior behavioral abilities in the blind, and the neural correlates associated with crossmodal neuroplasticity following visual deprivation.

Altered Cross-Modal Processing in the Primary Auditory Cortex of Congenitally Deaf Adults: A Visual-Somatosensory fMRI Study with a Double-Flash Illusion

The developing brain responds to the environment by using statistical correlations in input to guide functional and structural changes-that is, the brain displays neuroplasticity. Experience shapes brain development throughout life, but neuroplasticity is variable from one brain system to another. How does the early loss of a sensory modality affect this complex process? We examined cross-modal neuroplasticity in anatomically defined subregions of Heschl's gyrus, the site of human primary auditory cortex, in congenitally deaf humans by measuring the fMRI signal change in response to spatially coregistered visual, somatosensory, and bimodal stimuli. In the deaf Heschl's gyrus, signal change was greater for somatosensory and bimodal stimuli than that of hearing participants. Visual responses in Heschl's gyrus, larger in deaf than hearing, were smaller than those elicited by somatosensory stimulation. In contrast to Heschl's gyrus, in the superior-temporal cortex visual signal was comparable to somatosensory signal. In addition, deaf adults perceived bimodal stimuli differently; in contrast to hearing adults, they were susceptible to a double-flash visual illusion induced by two touches to the face. Somatosensory and bimodal signal change in rostrolateral Heschl's gyrus predicted the strength of the visual illusion in the deaf adults in line with the interpretation that the illusion is a functional consequence of the altered cross-modal organization observed in deaf auditory cortex. Our results demonstrate that congenital and profound deafness alters how vision and somatosensation are processed in primary auditory cortex.

Neural reorganization following sensory loss: the opportunity of change

There is growing evidence that sensory deprivation is associated with crossmodal neuroplastic changes in the brain. After visual or auditory deprivation, brain areas that are normally associated with the lost sense are recruited by spared sensory modalities. These changes underlie adaptive and compensatory behaviours in blind and deaf individuals. Although there are differences between these populations owing to the nature of the deprived sensory modality, there seem to be common principles regarding how the brain copes with sensory loss and the factors that influence neuroplastic changes. Here, we discuss crossmodal neuroplasticity with regards to behavioural adaptation after sensory deprivation and highlight the possibility of maladaptive consequences within the context of rehabilitation.

Cross-modal neuroplasticity in the blind mole rat Spalax ehrenbergi: a WGA-HRP tracing study.

Spalax ehrenbergi is a subterranean rodent possessing extremely degenerated eyes but a distinguishable dorsal lateral geniculate nucleus (dLGN) which projects ipsilaterally to a fair sized striate cortex. 2-Deoxyglucose and electrophysiological studies have shown that these areas are vigorously activated by auditory input. We show here, using the neuroanatomical tracer WGA-HRP, that the major source of the auditory input to the visual system is the inferior colliculus that, in addition to all its typical auditory targets, also projects to the dLGN. The visual thalamo-cortical pathway thereupon processes auditory information. This is the first naturally blind mammal in which the origin of auditory compensatory projections have been traced and described.