Patrice Voss

Organization and reorganization of sensory-deprived cortex.

The scientific literature has grown rich in research illustrating the remarkable ability of the brain to reorganize itself following sensory loss. In particular, visually deafferented regions within the occipital cortex of early blind individuals have been repeatedly shown to be functionally recruited to carry out a wide variety of nonvisual tasks. While the novelty of such a finding might be wearing off, more recent research has begun to examine whether this crossmodal takeover of the occipital cortex in blindness follows some sort of organizational principle. Here we first review the most recent evidence from neuroimaging studies that illustrate how the pre-existing functional specialization of cortical sub-regions appears to be preserved following sensory deprivation. We discuss and compare work on visual and auditory deprivation, as well as research on individuals with intact sensory systems. We suggest avenues for future exploration of these issues, such as identifying the neuroanatomical markers of crossmodal plasticity and elucidating the behavioral relevance of observed changes.

Occipital Cortical Thickness Predicts Performance on Pitch and Musical Tasks in Blind Individuals

The behavioral and neurofunctional consequences of blindness often include performance enhancements and recruitment of occipital regions for nonvisual tasks. How the neuroanatomical changes resulting from this sensory loss relate to these functional changes is, however, less clear. Previous studies using cortical thickness (CT) measures have shown thicker occipital cortex in early-blind (EB) individuals compared with sighted controls. We hypothesized that this finding reflects the crossmodal plasticity often observed in blind individuals and thus could reflect behavioral adaptations. To address this issue, CT measures in blind (early and late) and sighted subjects were obtained along with several auditory behavioral measures in an attempt to relate behavioral and neuroanatomical changes. Group contrasts confirmed previous results in showing thicker occipital cortex in the EB. Regression analyses between CT measures across the whole brain of all blind individuals with the behavioral scores from 2 tasks in which EB subjects were superior (pitch and melody discrimination) showed that CT of occipital areas was directly related to behavioral enhancements. These findings constitute a compelling demonstration that anatomical changes in occipital areas are directly related to heightened behavioral abilities in the blind and hence support the idea that these anatomical features reflect adaptive compensatory plasticity.

Sensitive and critical periods in visual sensory deprivation

While the demonstration of crossmodal plasticity is well established in congenital and early blind individuals, great debate still surrounds whether those who acquire blindness later in life can also benefit from such compensatory changes. No proper consensus has been reached despite the fact that a proper understanding of the developmental time course of these changes, and whether their occurrence is limited to—or within—specific time windows, is crucial to our understanding of the crossmodal phenomena. An extensive review of the literature reveals that while the majority of investigations to date have examined the crossmodal plasticity available to late blind individuals in quantitative terms, recent findings rather suggest that this reorganization also likely changes qualitatively compared to what is observed in early blindness. This obviously could have significant repercussions not only for the training and rehabilitation of blind individuals, but for the development of appropriate neuroprostheses designed to aid and potentially restore vision. Important parallels will also be drawn with the current state of research on deafness, which is particularly relevant given in the development of successful neuroprostheses (e.g., cochlear implants) for providing auditory input to the central nervous system otherwise aurally deafferented. Lastly, this paper will address important inconsistencies across the literature concerning the definition of distinct blind groups based on the age of blindness onset, and propose several alternatives to using such a categorization.

Relevance of Spectral Cues for Auditory Spatial Processing in the Occipital Cortex of the Blind

We have previously shown that some blind individuals can localize sounds more accurately than their sighted counterparts when one ear is obstructed, and that this ability is strongly associated with occipital cortex activity. Given that spectral cues are important for monaurally localizing sounds when one ear is obstructed, and that blind individuals are more sensitive to small spectral differences, we hypothesized that enhanced use of spectral cues via occipital cortex mechanisms could explain the better performance of blind individuals in monaural localization. Using positron-emission tomography (PET), we scanned blind and sighted persons as they discriminated between sounds originating from a single spatial position, but with different spectral profiles that simulated different spatial positions based on head-related transfer functions. We show here that a sub-group of early blind individuals showing superior monaural sound localization abilities performed significantly better than any other group on this spectral discrimination task. For all groups, performance was best for stimuli simulating peripheral positions, consistent with the notion that spectral cues are more helpful for discriminating peripheral sources. PET results showed that all blind groups showed cerebral blood flow increases in the occipital cortex; but this was also the case in the sighted group. A voxel-wise covariation analysis showed that more occipital recruitment was associated with better performance across all blind subjects but not the sighted. An inter-regional covariation analysis showed that the occipital activity in the blind covaried with that of several frontal and parietal regions known for their role in auditory spatial processing. Overall, these results support the notion that the superior ability of a sub-group of early-blind individuals to localize sounds is mediated by their superior ability to use spectral cues, and that this ability is subserved by cortical processing in the occipital cortex.

Evidence for both compensatory plastic and disuse atrophy-related neuroanatomical changes in the blind.

The behavioural and neurofunctional consequences of blindness are becoming increasingly well established, and it has become evident that the amount of reorganization is directly linked to the behavioural adaptations observed in the blind. However investigations of potential neuroanatomical changes resulting from blindness have yielded conflicting results as to the nature of the observed changes, because apparent loss of occipital tissue is difficult to reconcile with observed functional recruitment. To address this issue we used two complementary brain measures of neuroanatomy, voxel-based morphometry and magnetization transfer imaging, with the latter providing insight into myelin concentration through the magnetization transfer ratio. Both early and late blind, as well as sighted control subjects participated in the study and were tested on a series of auditory and tactile tasks to provide behavioural data that we could relate to neuroanatomy. The behavioural findings show that the early blind outperform the sighted in four of five tasks, whereas the late blind do so for only one. Moreover, correlations between the auditory and tactile performance of early blind individuals seem to indicate that they might benefit from some general-purpose compensatory plasticity mechanisms, as opposed to modality-specific ones. Neuroanatomical findings reveal three key findings: (i) occipital regions in the early blind have higher magnetization transfer ratio and grey matter concentration than in the sighted; (ii) behavioural performance of the blind is strongly predicted by magnetization transfer ratio and grey matter concentration in different occipital regions; and (iii) lower grey matter and white matter concentration was also found in other occipital areas in the early blind compared to the sighted. We thus show a clear dissociation between anatomical changes that are direct result of sensory deprivation and consequent atrophy, and those related to compensatory reorganization and behavioural adaptations. Moreover, the magnetization transfer ratio results also suggest that one mechanism for this reorganization may be related to increased myelination of intracortical neurons, or perhaps of fibres conveying information to and from remote locations.

Trade-Off in the Sound Localization Abilities of Early Blind Individuals between the Horizontal and Vertical Planes

There is substantial evidence that sensory deprivation leads to important cross-modal brain reorganization that is paralleled by enhanced perceptual abilities. However, it remains unclear how widespread these enhancements are, and whether they are intercorrelated or arise at the expense of other perceptual abilities. One specific area where such a trade-off might arise is that of spatial hearing, where blind individuals have been shown to possess superior monaural localization abilities in the horizontal plane, but inferior localization abilities in the vertical plane. While both of these tasks likely involve the use of monaural cues due to the absence of any relevant binaural signal, there is currently no proper explanation for this discrepancy, nor has any study investigated both sets of abilities in the same sample of blind individuals. Here, we assess whether the enhancements observed in the horizontal plane are related to the deficits observed in the vertical plane by testing sound localization in both planes in groups of blind and sighted persons. Our results show that the blind individuals who displayed the highest accuracy at localizing sounds monaurally in the horizontal plane are also the ones who exhibited the greater deficit when localizing in the vertical plane. These findings appear to argue against the idea of generalized perceptual enhancements in the early blind, and instead suggest the possibility of a trade-off in the localization proficiency between the two auditory spatial planes, such that learning to use monaural cues for the horizontal plane comes at the expense of using those cues to localize in the vertical plane.

Early visual deprivation changes cortical anatomical covariance in dorsal-stream structures

Early blind individuals possess thicker occipital cortex compared to sighted ones. Occipital cortical thickness is also predictive of performance on several auditory discrimination tasks in the blind, which suggests that it can serve as a neuroanatomical marker of auditory behavioural abilities. In light of this atypical relationship between occipital thickness and auditory function, we sought to investigate here the covariation of occipital cortical morphology in occipital areas with that of all other areas across the cortical surface, to assess whether the anatomical covariance with the occipital cortex differs between early blind and sighted individuals. We observed a reduction in anatomical covariance between the right occipital cortex and several areas of the visual dorsal stream in a group of early blind individuals relative to sighted controls. In a separate analysis, we show that the performance of the early blind in a transposed melody discrimination task was strongly predicted by the strength of the cortical covariance between the occipital cortex and intraparietal sulcus, a region for which cortical thickness in the sighted was previously shown to predict performance in the same task. These findings therefore constitute the first evidence linking altered anatomical covariance to early sensory deprivation. Moreover, since covariation of cortical morphology could potentially be related to anatomical connectivity or driven by experience-dependent plasticity, it could consequently help guide future functional connectivity and diffusion tractography studies.

The influence of vision on sound localization abilities in both the horizontal and vertical planes.

Numerous recent reports have suggested that individuals deprived of vision are able to develop heightened auditory spatial abilities. However, most such studies have compared the blind to blindfolded sighted individuals, a procedure that might introduce a strong performance bias. Indeed, while blind individuals have had their whole lives to adapt to this condition, sighted individuals might be put at a severe disadvantage when having to localize sounds without visual input. To address this unknown, we compared the sound localization ability of eight sighted individuals with and without a blindfold in a hemi-anechoic chamber. Sound stimuli were broadband noise delivered via two speaker arrays: a horizontal array with 25 loudspeakers (ranging from −90° to +90°; 7.5°) and a vertical array with 16 loudspeakers (ranging from −45° to +67.5°). A factorial design was used, where we compared two vision conditions (blindfold vs. non-blindfold), two sound planes (horizontal vs. vertical) and two pointing methods (hand vs. head). Results show that all three factors significantly interact with one another with regards to the average absolute deviation error. Although blindfolding significantly affected all conditions, it did more so for head-pointing in the horizontal plane. Moreover, blindfolding was found to increase the tendency to undershoot more eccentric spatial positions for head-pointing, but not hand-pointing. Overall, these findings suggest that while proprioceptive cues appear to be sufficient for accurate hand pointing in the absence of visual feedback, head pointing relies more heavily on visual cues in order to provide a precise response. It also strongly argues against the use of head pointing methodologies with blindfolded sighted individuals, particularly in the horizontal plane, as it likely introduces a bias when comparing them to blind individuals.

Dynamic Brains and the Changing Rules of Neuroplasticity: Implications for Learning and Recovery

A growing number of research publications have illustrated the remarkable ability of the brain to reorganize itself in response to various sensory experiences. A traditional view of this plastic nature of the brain is that it is predominantly limited to short epochs during early development. Although examples showing that neuroplasticity exists outside of these finite time-windows have existed for some time, it is only recently that we have started to develop a fuller understanding of the different regulators that modulate and underlie plasticity. In this article, we will provide several lines of evidence indicating that mechanisms of neuroplasticity are extremely variable across individuals and throughout the lifetime. This variability is attributable to several factors including inhibitory network function, neuromodulator systems, age, sex, brain disease, and psychological traits. We will also provide evidence of how neuroplasticity can be manipulated in both the healthy and diseased brain, including recent data in both young and aged rats demonstrating how plasticity within auditory cortex can be manipulated pharmacologically and by varying the quality of sensory inputs. We propose that a better understanding of the individual differences that exist within the various mechanisms that govern experience-dependent neuroplasticity will improve our ability to harness brain plasticity for the development of personalized translational strategies for learning and recovery following brain injury or disease.

Crossmodal Processing of Haptic Inputs in Sighted and Blind Individuals

In a previous behavioral study, it was shown that early blind individuals were superior to sighted ones in discriminating two-dimensional (2D) tactile angle stimuli. The present study was designed to assess the neural substrate associated with a haptic 2D angle discrimination task in both sighted and blind individuals. Subjects performed tactile angle size discriminations in order to investigate whether the pattern of crossmodal occipital recruitment was lateralized as a function of the stimulated hand. Task-elicited activations were also compared across different difficulty levels to ascertain the potential modulatory role of task difficulty on crossmodal processing within occipital areas. We show that blind subjects had more widespread activation within the right lateral and superior occipital gyri when performing the haptic discrimination task. In contrast, the sighted activated the left cuneus and lingual gyrus more so than the blind when performing the task. Furthermore, activity within visual areas was shown to be predictive of tactile discrimination thresholds in the blind, but not in the sighted. Activity within parietal and occipital areas was modulated by task difficulty, where the easier angle comparison elicited more focal occipital activity along with bilateral posterior parietal activity, whereas the more difficult comparison produced more widespread occipital activity combined with reduced parietal activation. Finally, we show that crossmodal reorganization within the occipital cortex of blind individuals was primarily right lateralized, regardless of the stimulated hand, supporting previous evidence for a right-sided hemispheric specialization of the occipital cortex of blind individuals for the processing of tactile and haptic inputs.