Review articleCrossmodal reorganisation in deafness: Mechanisms for functional preservation and functional change
Introduction
The study of deafness and blindness allows us to understand how the brain develops under different environmental conditions. In these cases, the variation is not in the environment per se, but in the types of sensory inputs that provide information about the environment. Understanding reorganisation in congenital deafness and blindness provides fundamental insights into brain function and its potential for change and enhancement, with important implications for the development of sensorimotor substitution devices and neural prostheses, for the planning of inclusive policies and for the design of better educational practices.
One of the most prominent questions on neural reorganisation concerns the function of sensory cortices when the preferred sensory input is missing. Studies in deaf and blind individuals have revealed significant reorganisation in sensory cortices as a consequence of sensory loss (Rauschecker, 1995; Bavelier and Neville, 2002; Merabet and Pascual-Leone, 2010; Ricciardi and Pietrini, 2011). In deaf individuals, the superior temporal cortex (STC), a region typically considered auditory, responds to other sensory inputs, such as vision and touch (Finney et al., 2001, 2003; MacSweeney et al., 2002; Fine et al., 2005; Auer et al., 2007; Emmorey et al., 2011; Leonard et al., 2012; Bottari et al., 2014; Karns et al., 2012; Cardin et al., 2013). In blind individuals, occipital regions usually involved in visual processing are activated by sound and touch (Arno et al., 2001; Amedi et al., 2002, 2007; Gougoux et al., 2005; Poirier et al., 2006; Collignon et al., 2007; Voss et al., 2008; Merabet et al., 2008). This type of reorganisation is known as crossmodal plasticity, where brain regions that usually process sensory information from a given modality adapt to process sensory information from a different modality (e.g. Rauschecker, 1995, 2002; Merabet and Pascual-Leone, 2010).
Several studies of deafness and blindness in animals and humans propose that one of the mechanisms of crossmodal plasticity is preservation of function, where cortical regions keep their original function but adapt to respond to a different sensory input (Pascual-Leone et al., 2005; Ricciardi et al., 2009; Lomber et al., 2010; Renier et al., 2013; Heimler et al., 2015). However, research in humans has also shown that sensory deprived regions take on higher-order cognitive functions such as working memory and language (Buchsbaum et al., 2015; Cardin et al., 2013; Ding et al., 2015; Röder et al., 2000, 2002; Watkins et al., 2012; Bedny et al., 2011, 2012, 2015; Bedny, 2017). Executive functions such as working memory are usually associated with activity in frontoparietal brain regions involved in cognitive control (D’Esposito and Postle, 2015), whereas the auditory and visual cortices are typically considered sensory regions. Thus, these findings raise the possibility of a change of function from sensory processing to executive functions, suggesting great malleability in the functional future of cortical areas. Researchers have referred to these theories in different ways, but here we summarise them into two main theoretical accounts, using a nomenclature that highlights function, the topic at the core of our discussion:
- 1
Functional Preservation: This theory proposes that after cross-modal reorganisation, cortical regions preserve the function they previously had, but adapt to process a sensory input in a different modality (Pascual-Leone et al., 2005; Ricciardi et al., 2009; Lomber et al., 2010; Renier et al., 2013; Heimler et al., 2015). For example, regions of the brain that in hearing cats are involved in sensory processing of auditory motion are involved in sensory processing of visual motion in deaf cats (Lomber et al., 2010). In both cases the function is the same -- motion -- but the modality of the input is different. This preservation is also observed for higher cognitive functions such as language, where superior temporal regions involved in speech processing in hearing individuals are recruited for sign language processing in deaf individuals, but not in hearing native signers (MacSweeney et al., 2002; Cardin et al., 2013, 2016a; Twomey et al., 2017).
- 2
Functional Change: This theory proposes a change in both the function of the cortex and the sensory modality to which it responds (see Bedny, 2017 for a review). For example, auditory sensory areas in hearing individuals respond to visual working memory in deaf individuals (Buchsbaum et al., 2015; Cardin et al., 2013; Ding et al., 2015), and visual occipital regions are involved in language processing in blindness (Röder et al., 2000, 2002; Watkins et al., 2012; Bedny et al., 2011, 2012, 2015; Bedny, 2017).
It has been challenging to converge these findings on a single theory because there is extensive experimental evidence supporting both functional preservation and functional change. In fact, in some cases, there is evidence supporting preservation and change in the same cortical region. In this review, we use examples from the study of deafness to discuss mechanisms that could explain evidence supporting both accounts in the same or adjacent cortical regions. We will start with a summary of the evidence from deafness and blindness supporting each theory, and then describe two specific examples from the study of deafness that provide evidence in support of preservation and change of function in the same portion of the posterior Superior Temporal Cortex (STC). We first concentrate on the left pSTC, exploring the physiological and anatomical changes that could explain both language and working memory effects. We then move onto considering whether a single functional reorganisation theory could explain both effects. In the last section, we use the right pSTC as an example to discuss whether effects are arising from independent but adjacent cortical regions. Our aim is to reconcile findings that may initially seem contradictory, and provide a theoretical framework with testable hypotheses for future research.
Section snippets
Evidence for functional preservation
Theories of functional preservation propose that crossmodal reorganisation results from cortical regions preserving the function they would usually have, but adapting to processing a different sensory modality (Amedi et al., 2002; Pascual-Leone et al., 2005; Ricciardi et al., 2009; Lomber et al., 2010; Renier et al., 2013; Heimler et al., 2015). In some accounts of this theory, researchers propose that crossmodal plasticity is a product of the brain being organised into processing modules that
Evidence for functional change
Functional change theories propose not only a change in the sensory modality recruiting a sensory deprived cortex, but fundamentally a change in the underlying function of this region (Uhl et al., 1991; Sadato et al., 1996; Cohen et al., 1997; Röder et al., 2002; Bedny et al., 2011; Burton et al., 2012; Lane et al., 2015; Bedny, 2017). In the case of deafness, evidence supporting this theory comes from the study of working memory in humans, where typically auditory regions are recruited for
Functional preservation and functional change in the same cortical region: the case of the deaf posterior Superior Temporal Cortex
The evidence summarised above suggests that crossmodal plasticity does not follow a single rule. It is likely that different brain regions undergo functional change or functional preservation depending on the weight and utility of outputs and inputs they receive, and the computations that are possible in such regions. Nonetheless, there are situations in which evidence for both these phenomena have been found in the same cortical area (Reich et al., 2011; Striem-Amit et al., 2012; Cardin et
Anatomical and physiological substrates for functional preservation and functional change
When discussing the anatomical and physiological mechanisms that could support functional preservation and functional change, it is important to consider certain anatomical and technical constraints. It is known that only a few new neuronal projections are found in crossmodally reorganised areas (Barone et al., 2013; Meredith et al., 2016; Meredith and Lomber, 2017). As such, plasticity likely arises from local and opportunistic changes such as unmasking of silent inputs, lack of pruning during
Different effects may reflect the same underlying function
Working memory and language findings in the deaf pSTC could be easily explained if both effects were a manifestation of the same underlying function. The most parsimonious interpretation for our present examples is that they both reflect either language or working memory activity.
We start by considering whether the working memory effects observed by Cardin et al. (2018) could be explained by labeling or phonological coding of the stimuli, which is a common strategy in working memory tasks (
Functional preservation and functional change may co-exist in adjacent, but distinct anatomical locations
Most of the evidence from humans discussed so far, and our two working examples, are fMRI results from group averages. However, it could be the case that an effect which seems to originate from the same cortical region, arises indeed from adjacent regions and merges into a single activation when smoothing and averaging are performed across participants. Plasticity effects in the right pSTC of deaf individuals can clearly exemplify why this is a potential issue in the study of deafness. Many
Can the same principles be applied to the study of blindness?
A detailed review of the literature on blindness is beyond the scope of this review, but it is important to consider whether the accounts discussed above can also explain potentially contradicting results in the literature on crossmodal plasticity in the blind brain. Evidence for functional change and functional preservation in the same region in blind individuals has been reported in the Visual Word Form Area (VWFA). This is a portion of the left ventral occipitotemporal cortex (VOTC), which
Conclusion and future directions
The study of plasticity in deaf and blind individuals has revealed a striking capacity of the brain for adaptation and change. Theories of crossmodal plasticity propose either a functional preservation or a functional change. Evidence from both sets of theories have made important contributions to our understanding of crossmodal reorganisation, but more generally to our knowledge of the brain, challenging traditional models of neural function. These include theories such as the
Acknowledgement
This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC; Project Reference: BB/P019994/1).
References (143)
- et al.
Occipital activation by pattern recognition in the early blind using auditory substitution for vision
Neuroimage
(2001) - et al.
Touch, sound and vision in human superior temporal sulcus
Neuroimage
(2008) Evidence from blindness for a cognitively pluripotent cortex
Trends Cogn. Sci. (Regul. Ed.)
(2017)- et al.
A sensitive period for language in the visual cortex: distinct patterns of plasticity in congenitally versus late blind adults
Brain Lang.
(2012) - et al.
White matter connectivity between occipital and temporal regions involved in face and voice processing in hearing and early deaf individuals
Neuroimage
(2018) - et al.
Visual change detection recruits auditory cortices in early deafness
Neuroimage
(2014) - et al.
Immature frontal lobe contributions to cognitive control in children: evidence from fMRI
Neuron.
(2002) - et al.
Recognition memory for Braille or spoken words: an fMRI study in early blind
Brain Res.
(2012) - et al.
Origins of thalamic and cortical projections to the posterior auditory field in congenitally-deaf cats
Hear. Res.
(2017) - et al.
Superior temporal activation as a function of linguistic knowledge: insights from deaf native signers who speechread
Brain Lang.
(2010)
Differential activity in Heschl’s gyrus between deaf and hearing individuals is due to auditory deprivation rather than language modality
Neuroimage.
Specialization within the ventral stream: the case for the visual word form area
Neuroimage
The reorienting system of the human brain: from environment to theory of mind
Neuron
Sign language processing and the mirror neuron system
Cortex
Hemispheric specialization for ASL signs and English words: differences between imageable and abstract forms
Neuropsychologia
Neural systems underlying lexical retrieval for sign language
Neuropsychologia
The neural correlates of sign versus word production
NeuroImage
Neural responses to meaningless pseudosigns: evidence for sign-based phonetic processing in superior temporal cortex
Brain Lang.
Right temporoparietal junction activation by a salient contextual cue facilitates target discrimination
Neuroimage.
Modality-independent encoding of individual concepts in the left parietal cortex
Neuropsychologia.
Origins of task-specific sensory-independent organization in the visual and auditory brain: neuroscience evidence, open questions and clinical implications
Curr. Opin. Neurobiol.
Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis
Neuropsychol.
Origin of the thalamic projection to dorsal auditory cortex in hearing and deafness
Hear. Res.
Word selectivity in high-level visual cortex and reading skill
Dev. Cogn. Neurosci.
Dissociating linguistic and nonlinguistic gestural communication in the brain
Neuroimage
The signing brain: the neurobiology of sign language
Trends. Cogn. Sci.
The visual word form area: expertise for reading in the fusiform gyrus
Trends Cogn Sci
Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats
Hear. Res.
Species-dependent role of crossmodal connectivity among the primary sensory cortices
Hear. Res.
Cortical and thalamic connectivity of the auditory ectosylvian cortex of early deaf cats: implications for neural mechanisms of crossmodal plasticity
Hear. Res.
Attention to central and peripheral visual space in a movement detection task: an event-related potential and behavioral study. II. Congenitally deaf adults
Brain Res.
Decoding visual location from neural patterns in the auditory cortex of the congenitally deaf
Psychol. Sci.
Convergence of visual and tactile shape processing in the human lateral occipital complex
Cereb. Cortex
Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind
Nat. Neurosci.
Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects
Nat. Neurosci.
Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex
Nat. Neurosci.
Vibrotactile activation of the auditory cortices in deaf versus hearing adults
Neuroreport
Reorganization of the connectivity of cortical field DZ in congenitally deaf cat
PLoS One
Laminar mechanisms for working memory
Proc. Natl. Acad. Sci.
Cross-modal plasticity: where and how? Nat
Rev. Neurosci.
Hemispheric specialization for English and ASL: left invariance-right variability
Neuroreport
Language processing in the occipital cortex of congenitally blind adults
Proc. Natl. Acad. Sci.
Visual” cortex responds to spoken language in blind children
J. Neurosci.
Functional selectivity for face processing in the temporal voice area of early deaf individuals
Proc. Natl. Acad. Sci.
Congenital deafness affects deep layers in primary and secondary auditory cortex
J. Comp. Neurol.
Task-specific reorganization of the auditory cortex in deaf humans
Proc. Natl. Acad. Sci.
Tactile spatial working memory activates the dorsal extrastriate cortical pathway in congenitally blind individuals
Arch. Ital. Biol.
Neural substrates for verbal working memory in deaf signers: fMRI study and lesion case report
Brain Lang.
Adaptive changes in early and late blind: a fMRI study of braille reading
J. Neurophysiol.
Functional and structural changes throughout the auditory system following congenital and early-onset deafness: implications for hearing restoration
Front. Syst. Neurosci.
Cited by (29)
Connectome alterations following perinatal deafness in the cat
2024, NeuroImageEvent-related potential correlates of visuo-tactile motion processing in congenitally deaf humans
2022, NeuropsychologiaCitation Excerpt :In contrast, comparably little is known about the impact of deafness on the development of multisensory processing. So far, most studies on neural plasticity in deaf individuals have focused on the visual modality (e.g., Neville and Lawson, 1987a, 1987b; for reviews see Bavelier et al., 2006; Cardin et al., 2020; Pavani and Bottari, 2012). An enhancement of visual processing abilities in deaf individuals has been observed most frequently, but not exclusively, for stimuli presented in the periphery or peri-foveal regions (Neville and Lawson, 1987b; for reviews see Bavelier et al., 2006; Pavani and Bottari, 2012).
Multisensory temporal processing in early deaf
2021, NeuropsychologiaCitation Excerpt :Right pSTS showed increased recruitment for tactile motion in ED individuals (Scurry, Huber, et al., 2020). Overlap of visual and somatosensory responses in right pSTS of ED individuals suggested altered neural architecture for multisensory or high-order multimodal function, e.g., attentional processing (Cardin et al., 2020). Multisensory temporal processing in the pSTS has not been specifically investigated in ED.