One of the most significant effects of neural plasticity manifests in the case of sensory deprivation when cortical areas that were originally specialized for the functions of the deprived sense take over the processing of another modality. Vision and audition represent two important senses needed to navigate through space and time. Therefore, the current systematic review discusses the cross-modal behavioral and neural consequences of deafness and blindness by focusing on spatial and temporal processing abilities, respectively. In addition, movement processing is evaluated as compiling both spatial and temporal information. We examine whether the sense that is not primarily affected changes in its own properties or in the properties of the deprived modality (i.e., temporal processing as the main specialization of audition and spatial processing as the main specialization of vision). References to the
Previous reviews addressed various effects of neural plasticity in blindness or deafness (e.g., [ Recruitment of the cortical area associated with the deprived sense (i.e., in blindness, the occipital cortex for vision, and in deafness, the temporal cortex for audition) results in superior performance in its initial specialization: Auditory spatial processing will be enhanced in blindness (Figure Visual temporal processing will be enhanced in deafness (Figure Recruitment of the cortical area associated with the deprived sense results in superior performance in the specialization of the overtaking sense: Auditory temporal processing will be enhanced in blindness (Figure Visual spatial processing will be enhanced in deafness (Figure
Illustration of the possible consequences of cross-modal reorganization following sensory deprivation. In typically developed individuals, the occipital cortex executes the highly detailed spatial processing of visual stimuli, whereas the temporal cortex is adequately used for the high temporal processing of auditory stimuli. Following blindness, (a) an improvement in spatial auditory processing abilities and/or (b) an improvement in temporal auditory processing abilities occurs through the takeover of certain regions in the occipital cortex (hatched area). Following deafness, (c) an improvement in spatial visual processing abilities and/or (d) an improvement in temporal visual processing abilities occurs through the takeover of certain regions in the temporal cortex (hatched area). Notably, outcomes (a) and (b), as well as (c) and (d), are not necessarily mutually exclusive. Additionally, certain aspects of sensory processing are plausibly decreased after cortical reorganization, as indicated by the asterisks. Hypothesized subsequent behavioral outcomes are shown on the right side of the figure.
Figure
Researchers examining deaf cats proposed a theory for plasticity-related reorganization principles that limits the functions affected by plasticity [
Theories about brain organization and neural plasticity. Theories are outlined and categorized as general cortical organization principles, directional hypotheses of the neural plasticity-induced effects and theories that state which functions are likely affected. A further description of the theories and a reference to corresponding publications is provided in the main text.
Relating these reorganization principles to the hypotheses formulated above, the current systematic review has two main aims. First, regarding the metamodal organization principle and the prior specialization of each sense, we will explore whether specializations of the deprived or overtaking sense are primarily altered (Figure
The PubMed database was searched using single keywords and keyword combinations of the abstract/titles of the available articles listed in Supplementary Table
The abstracts of those 531 articles were screened. For inclusion, studies were required to address either the spatial or temporal auditory abilities of blind individuals, the spatial or temporal visual abilities of deaf individuals, or visual/auditory motion processing. Whenever an abstract did not contain sufficient information, the methods, in particular the tasks assigned, were evaluated. Importantly, studies addressing language or speech processing, as well as word recognition, were excluded. Higher-order processing involving language and memory was not in the scope of the current review. Controlling for language is particularly difficult, since previous studies rarely assessed the language experience and proficiency of participants or compared deaf children born to deaf parents with deaf children born to hearing parents. The importance of language experience is stressed elsewhere (e.g., see a comment by MacSweeney and Cardin [
Flow diagram of the systematic search strategy. The search strategy and selection of the articles are illustrated as a stepwise process.
Due to visual deprivation, blind individuals rely strongly on their remaining senses to orient in space and to navigate through their environment. Consequently, numerous studies have addressed the question whether blind individuals exhibit altered spatial localization abilities in the remaining senses. Referring to Figure
While no differences in accuracy were observed when assessing
In addition to horizontal and vertical localization,
Similarly,
Finally, uniting all spatial aspects,
Several studies identified a link between enhanced behavioral performance and visual cortex recruitment. Based on electroencephalography (EEG) investigations, congenitally blind individuals display greater accuracy when
Although increased activation of the right occipital cortex is thus often reported, increased behavioral performance is not always found (e.g., [
Finally, virtual acoustics, i.e., the simulation of sound appearing from different locations played via headphones, enables investigations of the underlying neural mechanisms in more natural paradigms. It provides a possibility to circumvent the limitations derived from some imaging techniques, such as fMRI. However, no behavioral differences were reported in the few studies using virtual acoustics, although, again, early blind individuals recruited posterior parietal areas and the (right) middle occipital gyrus for sound localization, with the latter being related to performance [
In contrast to the well-studied spatial auditory abilities of blind individuals, less evidence for similar effects on temporal processing abilities is available (see Figure
Within the context of
In contrast to the behavioral study by Lerens et al. [
In real world environments, auditory stimuli often are not static but rather move in space and change dynamically. Without visual input, blind individuals must rely more on auditory motion localization, namely, the ongoing encoding of temporally ordered spatial auditory cues.
The importance of vision in
Using a 2-dimensional setup requiring the
Even after cataract treatment and
Despite the lack of a behavioral difference between blind and sighted individuals in two-alternative forced choice tasks assessing
Similarly, studies assessing auditory
Notably, while this additive shift was apparent across a variety of tasks, it often only applied to
Moreover, neural plasticity related to
Finally, consistent with the results of the behavioral studies, cross-modal neural adaptations appear to occur, even during short phases of congenital blindness, followed by (partial)
Taken together, the direction of the effect of neural plasticity strongly depends on the experimental setup. As previously suggested [
Corresponding neural studies often linked the increased visuospatial performance (Figure
Consequences of visual and auditory deprivation. Summary of the behavioral and neural results of the reported studies addressing visual and auditory deprivation. The major findings for spatial, temporal, and movement processing are depicted separately, and the hypotheses listed in Figure
After considering both spatial and temporal processing in blind individuals, we will now elaborate plasticity-related alterations in visual spatial and temporal processing occurring following auditory deprivation. Importantly, similar to the behavioral results obtained from blind individuals, the reported changes in performance in studies examining behavior alone (without any neural measures) might be due to cross-modal alterations, as well as intracortical changes and/or alterations within the sensory organs. Additionally, most studies related to deafness have investigated perceptual abilities after hearing restoration through cochlear implantation and (dis)advantages of cross-modal plasticity that affect or even prevent hearing rehabilitation (e.g., for a recent review, see [
Nonetheless, visual spatial processing in deaf individuals (Figure
Previous studies concluded that deafness leads to an increased sensitivity of spatial processing abilities in the periphery [
Visual attention appears to develop differently in hearing and deaf children [
Similarly, outcomes of studies with deaf adults vary depending on the age range, stimuli, and task administered. For example, a study in young adults (18-40 years of age) was unable to replicate a previous investigation showing enhanced spatial performance in the periphery in participants aged greater than 13 years [
Studies investigating the link between altered
Compared to various behavioral studies addressing the spatial (attention) domain, only a few studies have investigated temporal visual processing in deaf individuals (Figure
The accuracy of detecting the correct visual
In addition to the altered visual attention distribution, some deficits in auditory temporal duration perception were reported following deafness. Deaf individuals’
Similar to the auditory studies conducted in blind individuals, many neural studies investigating deafness did not report any behavioral differences. Technical issues or task selection might have influenced the results [
Another insight into possible temporally and spatially related behavioral and cortical changes is provided by studies investigating visual motion processing in deaf individuals. The temporal judgment of moving objects might be more relevant in daily life situations, e.g., when catching a ball or evading a moving obstacle, rather than determining the temporal order of an event with high temporal accuracy. Studies investigating visual motion processing might thus delineate a distinct natural testing environment.
Intuitively, deaf individuals would be equipped with better visual motion processing to compensate for the loss of auditory information that might have provided assisting information. Surprisingly, in early investigations, deaf individuals did not outperform hearing individuals in
Structural changes, such as changes in cortical thickness or myelination, as well as alterations in functional connectivity during the passive observation of visual motion might be linked to better motion detection [
Most studies explored the consequences of auditory deprivation on spatial processing (Figure
Few imaging studies have linked the enhanced performance of deaf individuals on spatial visual processing in the periphery (Figure
The aim of the current review was to identify whether cross-modal plasticity is linked to enhancements or deficits in processes in which the deprived and/or the overtaking sense specializes. Furthermore, we investigated whether these alterations fit into the framework of previously proposed reorganization principles.
Some similarities become apparent between visual and auditory deprivations. First, in both types of sensory deprivation, enhanced processing of peripheral stimuli has often been reported. This finding contrasts results observed in sighted and hearing individuals who mainly favor the central field. Nonsensory-deprived individuals likely utilize the integration of information from multiple senses to efficiently perceive the entire spatial environment [
Taken together, the spatial domain (specialization of vision, Figures
Some remarks about these investigations of neural plasticity and their clinical implications are necessary. First, multiple terms for the same or similar phenomena have been used in previous studies of cross-modal plasticity. For example, the
Next, although the cross-modal takeover appears to follow strict functional rules that are consistent with the theories described in this review, these findings should not be translated to each case of sensory loss. Multiple factors impair the generalization of the outcomes and make cross-modal plasticity a highly individualized phenomenon. Thus, caution is warranted when comparing various studies of neural plasticity. On a fairly basic level, for example, plastic reorganizations of the brain due to damage or deprivation of a sense might largely differ from adaptations of the brain caused by experience and the learning of new skills. Various forms and degrees of plasticity have been observed in previous studies [
Types of plasticity and influencing factors
Type | Function |
(1) Strengthening of cognitive functions | Skill learning (e.g., [ |
(2) Hemispherectomy | Removal of one hemisphere to treat a variety of seizure disorders, leading to a takeover of functions that were initially performed by or in combination with the removed hemisphere (e.g., [ |
(3) Sensory substitution | Compensation of sensory loss by another sense or external device (e.g., [ |
(4) Early deprivation | Early loss due to a genetic or medical condition leading to compensation and broad takeover by other senses, although functional topography appears inert as dual streams (dorsal and ventral) remain intact; reorganization mainly occurs through bottom-up processing (e.g., [ |
(5) Late deprivation | Rather supportive in nature; compensation for the loss is restricted due to initial pruning and functional reorganization; rather through top-down processes (e.g., [ |
(6) Site of plastic changes | Cross-modal, intracortical, or even within the sensory organ (e.g., the retina [ |
Influencing factors | |
(1) Sensitive/critical periods | |
(2) Other senses and their critical periods [ | |
(3) Age of onset of deprivation | |
(4) Duration of deprivation | |
(5) Degree of loss [ | |
(6) Cause of sensory deprivation | |
(7) Working memory, intelligence quotient, gender (…) (e.g., see also the Ease of Language Understanding (ELU) model [ |
Moreover, several processing differences exist in the visual and auditory systems [
Although not all adaptations following cross-modal plasticity are either advantageous or disadvantageous, the reviewed findings may be helpful for future investigations or interventions. For example, noninvasive neural stimulation, techniques to enhance neural plasticity, and advantageous behaviors might be most effective in studies focusing on brain areas and connectivity involved in task-specific processes. Similarly, when developing sensory-substitution devices, i.e., the compensation for sensory loss by another sense through technical devices (e.g., hearing through a device that translates speech into tactile patterns), the notion of spatial and temporal processing enhancements in blind and deaf individuals, respectively, might guide technical developments to obtain suitable devices assisting individuals with tasks in daily life. Future virtual acoustic reality investigations might assist in realistic explorations of plasticity-induced effects (e.g., see [
The systematically outlined behavioral and neural findings provide a new framework to investigate how specific aspects of sensory processing are altered in blind and deaf individuals. Importantly, a clear overlap of the consequences of auditory and visual deprivation was observed. Various investigations primarily revealed alterations in spatial processing, allowing enhanced perception of the spatial environment after sensory deprivation. Future research investigating temporal auditory processing in blind individuals and temporal visual processing in deaf individuals are warranted to obtain a complete picture of the rules shaping cross-modal plasticity. Generally, behavioral performance is adapted in processes for which the overtaking and the deprived modality provide adequate resources. A modification mainly in the peripheral field and the right hemisphere of the brain becomes apparent. Concisely, these findings support a more sensory-unspecific but task- and principle-organized structure of the brain, which persists after sensory deprivation. This framework will likely be of high relevance for the development of sensory substitution devices and future investigations utilizing noninvasive brain stimulation.
The authors declare that there is no conflict of interest regarding the publication of this paper.
This work was supported by the Excellence Initiative of the German Federal and State Governments (ERS Boost Fund 2014; OPBF090) and by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation - Projektnummer 269953372/GRK2150). We would like to acknowledge Pixabay (
Table S1: keywords and paired keywords for the systematic literature review.
Table S2: overview of included studies per sensory deprivation and spatial/temporal process.