The effect of hearing loss on age-related differences in neural distinctiveness.

Age differences in cognitive performance have been shown to be overestimated if age-related hearing loss is not taken into account. Here, we investigated the role of age-related hearing loss on age differences in functional brain organization by assessing its impact on previously reported age differences in neural differentiation. To this end, we analyzed the data of 36 younger adults, 21 older adults with clinically normal hearing, and 21 older adults with mild-to-moderate hearing loss who had taken part in a functional localizer task comprising visual (i.e., faces, scenes) and auditory stimuli (i.e., voices, music) while undergoing functional magnetic resonance imaging. Evidence for reduced neural distinctiveness in the auditory cortex was observed only in older adults with hearing loss relative to younger adults, whereas evidence for reduced neural distinctiveness in the visual cortex was observed both in older adults with normal hearing and in older adults with hearing loss relative to younger adults. These results indicate that age-related dedifferentiation in the auditory cortex is exacerbated by age-related hearing loss.

Sight restoration in congenitally blind humans does not restore visual brain structure.

It is unknown whether impaired brain structure after congenital blindness is reversible if sight is restored later in life. Using structural magnetic resonance imaging, visual cortical surface area and cortical thickness were assessed in a large group of 21 sight-recovery individuals who had been born blind and who months or years later gained sight through cataract removal surgery. As control groups, we included 27 normally sighted individuals, 10 individuals with permanent congenital blindness, and 11 sight-recovery individuals with a late onset of cataracts. Congenital cataract-reversal individuals had a lower visual cortical surface area and a higher visual cortical thickness than normally sighted controls. These results corresponded to those of congenitally permanently blind individuals suggesting that impaired brain structure did not recover. Crucially, structural brain alterations in congenital-cataract reversal individuals were associated with a lower post-surgery visual acuity. No significant changes in visual cortex structure were observed in sight-recovery individuals with late onset cataracts. The results demonstrate that impaired structural brain development due to visual deprivation from birth is not fully reversible and limits functional recovery. Additionally, they highlight the crucial importance of prevention measures in the context of other types of aberrant childhood environments including low socioeconomic status and adversity.

Top-down modulation of visual cortical processing after transient congenital blindness.

Early visual experience has been shown to be critical for the development of visual and multisensory functions; however, its impact on functional brain organization remains largely unexplored. Here, we therefore investigated the effect of early visual deprivation on top-down attentional modulation of visual cortical processing within the occipito-temporal cortex. Furthermore, we explored whether early visual deprivation may affect the extent to which typically visual, motion-selective area hMT responds to moving visual stimuli. Using functional magnetic resonance imaging, we compared cortical responses in area hMT and in the fusiform face area (FFA) to moving face stimuli - which were either task relevant or task irrelevant - relative to stationary face stimuli between cataract-reversal participants and normally sighted controls. Although both groups exhibited significantly stronger visual cortical responses in area hMT to moving stimuli than during the stationary baseline, the magnitude of this effect was significantly lower in the cataract-reversal group. In contrast, both groups exhibited significantly enhanced visual cortical responses in area hMT and in the FFA when moving face stimuli were task relevant compared to when they were task irrelevant, with no significant differences between groups in the magnitude of these effects. These results indicate that top-down attentional modulation of visual cortical processing in area hMT and FFA does not depend on early visual experience. Furthermore, the present results suggest that the functional specialization of area hMT for visual motion processing may be partially disrupted by early visual deprivation.

Audiovisual spatial recalibration but not integration is shaped by early sensory experience.

To clarify the role of sensory experience during early development for adult multisensory learning capabilities, we probed audiovisual spatial processing in human individuals who had been born blind because of dense congenital cataracts (CCs) and who subsequently had received cataract removal surgery, some not before adolescence or adulthood. Their ability to integrate audio-visual input and to recalibrate multisensory spatial representations was compared to normally sighted control participants and individuals with a history of developmental (later onset) cataracts. Results in CC individuals revealed both normal multisensory integration in audiovisual trials (ventriloquism effect) and normal recalibration of unimodal auditory localization following audiovisual discrepant exposure (ventriloquism aftereffect) as observed in the control groups. In addition, only the CC group recalibrated unimodal visual localization after audiovisual exposure. Thus, in parallel to typical multisensory integration and learning, atypical crossmodal mechanisms coexisted in CC individuals, suggesting that multisensory recalibration capabilities are defined during a sensitive period in development.

Typical resting-state activity of the brain requires visual input during an early sensitive period.

Sensory deprivation, following a total loss of one sensory modality e.g. vision, has been demonstrated to result in compensatory plasticity. It is yet not known to which extent neural changes, e.g. higher resting-state activity in visual areas (cross-modal plasticity) as a consequence of blindness, reverse, when sight is restored. Here, we used functional MRI to acquire blood oxygen level-dependent resting-state activity during an eyes open and an eyes closed state in congenital cataract-reversal individuals, developmental cataract-reversal individuals, congenitally permanently blind individuals and sighted controls. The amplitude of low frequency fluctuation of the blood oxygen level-dependent signal-a neural marker of spontaneous brain activity during rest-was analyzed. In accordance with previous reports, in normally sighted controls we observed an increase in amplitude of low-frequency fluctuation during rest with the eyes open compared with rest with eyes closed in visual association areas and in parietal cortex but a decrease in auditory and sensorimotor regions. In congenital cataract-reversal individuals, we found an increase of the amplitude of slow blood oxygen level-dependent fluctuations in visual cortex during rest with eyes open compared with rest with eyes closed too but this increase was larger in amplitude than in normally sighted controls. In contrast, congenital cataract-reversal individuals lagged a similar increase in parietal regions and did not show the typical decrease of amplitude of low-frequency fluctuation in auditory cortex. Congenitally blind individuals displayed an overall higher amplitude in slow blood oxygen level-dependent fluctuations in visual cortex compared with sighted individuals and compared with congenital cataract-reversal individuals in the eyes closed condition. Higher amplitude of low-frequency fluctuation in visual cortex of congenital cataract-reversal individuals than in normally sighted controls during eyes open might indicate an altered excitatory-inhibitory balance of visual neural circuits. By contrast, the lower parietal increase and the missing downregulation in auditory regions suggest a reduced influence of the visual system on multisensory and the other sensory systems after restoring sight in congenitally blind individuals. These results demonstrate a crucial dependence of visual and multisensory neural system functioning on visual experience during a sensitive phase in human brain development.

The effect of congenital blindness on resting-state functional connectivity revisited.

Lower resting-state functional connectivity (RSFC) between 'visual' and non-'visual' neural circuits has been reported as a hallmark of congenital blindness. In sighted individuals, RSFC between visual and non-visual brain regions has been shown to increase during rest with eyes closed relative to rest with eyes open. To determine the role of visual experience on the modulation of RSFC by resting state condition-as well as to evaluate the effect of resting state condition on group differences in RSFC-, we compared RSFC between visual and somatosensory/auditory regions in congenitally blind individuals (n = 9) and sighted participants (n = 9) during eyes open and eyes closed conditions. In the sighted group, we replicated the increase of RSFC between visual and non-visual areas during rest with eyes closed relative to rest with eyes open. This was not the case in the congenitally blind group, resulting in a lower RSFC between 'visual' and non-'visual' circuits relative to sighted controls only in the eyes closed condition. These results indicate that visual experience is necessary for the modulation of RSFC by resting state condition and highlight the importance of considering whether sighted controls should be tested with eyes open or closed in studies of functional brain reorganization as a consequence of blindness.

The size-weight illusion is unimpaired in individuals with a history of congenital visual deprivation.

Visual deprivation in childhood can lead to lifelong impairments in multisensory processing. Here, the Size-Weight Illusion (SWI) was used to test whether visuo-haptic integration recovers after early visual deprivation. Normally sighted individuals perceive larger objects to be lighter than smaller objects of the same weight. In Experiment 1, individuals treated for dense bilateral congenital cataracts (who had no patterned visual experience at birth), individuals treated for developmental cataracts (who had patterned visual experience at birth, but were visually impaired), congenitally blind individuals and normally sighted individuals had to rate the weight of manually explored cubes that differed in size (Small, Medium, Large) across two possible weights (350 g, 700 g). In Experiment 2, individuals treated for dense bilateral congenital cataracts were compared to sighted individuals in a similar task using a string set-up, which removed haptic size cues. In both experiments, indistinguishable SWI effects were observed across all groups. These results provide evidence that early aberrant vision does not interfere with the development of the SWI, and suggest a recovery of the integration of size and weight cues provided by the visual and haptic modality.

Neural mechanisms of visual sensitive periods in humans.

Sensitive periods in brain development are phases of enhanced susceptibility to experience. Here we discuss research from human and non-human neuroscience studies which have demonstrated a) differences in the way infants vs. adults learn; b) how the brain adapts to atypical conditions, in particular a congenital vs. a late onset blindness (sensitive periods for atypical brain development); and c) the extent to which neural systems are capable of acquiring a typical brain organization after sight restoration following a congenital vs. late phase of pattern vision deprivation (sensitive periods for typical brain development). By integrating these three lines of research, we propose neural mechanisms characteristic of sensitive periods vs. adult neuroplasticity and learning.

The Neural Correlates of Visual and Auditory Cross-Modal Selective Attention in Aging.

Age-related deficits in selective attention have been demonstrated to depend on the sensory modality through which targets and distractors are presented. Some of these investigations suggest a specific impairment of cross-modal auditory selective attention. For the first time, this study is taking on a whole brain approach while including a passive perception baseline, to investigate the neural underpinnings of selective attention across age groups, and taking the sensory modality of relevant and irrelevant (i.e., distracting) stimuli into account. Sixteen younger (mean age = 23.3 years) and 14 older (mean age = 65.3 years), healthy participants performed a series of delayed match-to-sample tasks, in which participants had to selectively attend to visual stimuli, selectively attend to auditory stimuli, or passively view and hear both types of stimuli, while undergoing 3T fMRI. The imaging analyses showed that areas recruited by cross-modal visual and auditory selective attention in both age groups included parts of the dorsal attention and frontoparietal control networks (i.e., intraparietal sulcus, insula, fusiform gyrus, anterior cingulate, and inferior frontal cortex). Most importantly, activation throughout the brain did not differ across age groups, suggesting intact brain function during cross-modal selective attention in older adults. Moreover, stronger brain activation during cross-modal visual vs. cross-modal auditory selective attention was found in both age groups, which is consistent with earlier accounts of visual dominance. In conclusion, these results do not support the hypothesized age-related deficit of cross-modal auditory selective attention. Instead, they suggest that the underlying neural correlates of cross-modal selective attention are similar in younger and older adults.

Disregarding hearing loss leads to overestimation of age-related cognitive decline.

Aging is associated with cognitive and sensory decline. While several studies have indicated greater cognitive decline among older adults with hearing loss, the extent to which age-related differences in cognitive processing may have been overestimated due to group differences in sensory processing has remained unclear. We addressed this question by comparing younger adults, older adults with good hearing, and older adults with poor hearing in several cognitive domains: working memory, selective attention, processing speed, inhibitory control, and abstract reasoning. Furthermore, we examined whether sensory-related cognitive decline depends on cognitive demands and on the sensory modality used for assessment. Our results revealed that age-related cognitive deficits in most cognitive domains varied as a function of hearing loss, being more pronounced in older adults with poor hearing. Furthermore, sensory-related cognitive decline was observed across different levels of cognitive demands and independent of the sensory modality used for cognitive assessment, suggesting a generalized effect of age-related hearing loss on cognitive functioning. As most cognitive aging studies have not taken sensory acuity into account, age-related cognitive decline may have been overestimated.

Persisting Cross-Modal Changes in Sight-Recovery Individuals Modulate Visual Perception.

Recent neuroimaging studies have demonstrated that a brief period of congenital blindness induces long-lasting reorganization within the visual cortex of sight-recovery humans [1, 2]. However, the behavioral consequences of this cross-modal reorganization are not yet known. Here we investigated this question by examining the transfer of motion aftereffects across the visual and auditory modalities within six individuals who had been born blind due to dense bilateral cataracts and regained sight when they were treated at 5-24 months of age. Cataract-reversal individuals were compared to normally sighted participants and-to distinguish between the effects of early visual deprivation and residual visual impairments-to an additional group of individuals who had had pattern vision in childhood but later developed visual impairments. Cataract-reversal individuals-but not normally sighted or visually impaired participants-exhibited a significant visual motion aftereffect following adaptation to auditory motion. Despite this, cataract-reversal individuals were as likely as individuals in either control group to show a significant auditory motion aftereffect following adaptation to visual motion. These results extend previous findings of persisting cross-modal reorganization within the typically visual motion-selective area hMT+/V5 in sight-recovery individuals [3, 4], by providing the first demonstration that cross-modal adaptation to a brief phase of congenital blindness has behaviorally relevant consequences for visual perceptual recovery.

Selective Attention and Sensory Modality in Aging: Curses and Blessings.

The notion that selective attention is compromised in older adults as a result of impaired inhibitory control is well established. Yet it is primarily based on empirical findings covering the visual modality. Auditory and especially, cross-modal selective attention are remarkably underexposed in the literature on aging. In the past 5 years, we have attempted to fill these voids by investigating performance of younger and older adults on equivalent tasks covering all four combinations of visual or auditory target, and visual or auditory distractor information. In doing so, we have demonstrated that older adults are especially impaired in auditory selective attention with visual distraction. This pattern of results was not mirrored by the results from our psychophysiological studies, however, in which both enhancement of target processing and suppression of distractor processing appeared to be age equivalent. We currently conclude that: (1) age-related differences of selective attention are modality dependent; (2) age-related differences of selective attention are limited; and (3) it remains an open question whether modality-specific age differences in selective attention are due to impaired distractor inhibition, impaired target enhancement, or both. These conclusions put the longstanding inhibitory deficit hypothesis of aging in a new perspective.

The Effect of Early Visual Deprivation on the Neural Bases of Auditory Processing.

Transient congenital visual deprivation affects visual and multisensory processing. In contrast, the extent to which it affects auditory processing has not been investigated systematically. Research in permanently blind individuals has revealed brain reorganization during auditory processing, involving both intramodal and crossmodal plasticity. The present study investigated the effect of transient congenital visual deprivation on the neural bases of auditory processing in humans. Cataract-reversal individuals and normally sighted controls performed a speech-in-noise task while undergoing functional magnetic resonance imaging. Although there were no behavioral group differences, groups differed in auditory cortical responses: in the normally sighted group, auditory cortex activation increased with increasing noise level, whereas in the cataract-reversal group, no activation difference was observed across noise levels. An auditory activation of visual cortex was not observed at the group level in cataract-reversal individuals. The present data suggest prevailing auditory processing advantages after transient congenital visual deprivation, even many years after sight restoration. SIGNIFICANCE STATEMENT: The present study demonstrates that people whose sight was restored after a transient period of congenital blindness show more efficient cortical processing of auditory stimuli (here speech), similarly to what has been observed in congenitally permanently blind individuals. These results underscore the importance of early sensory experience in permanently shaping brain function.

Increased visual cortical thickness in sight-recovery individuals.

Individuals who are born blind due to dense bilateral cataracts and who later regain vision due to cataract surgery provide a unique model to evaluate the effect of early sensory experience in humans. In recent years, several studies have started to assess the functional consequences of early visual deprivation in these individuals, revealing a number of behavioral impairments in visual and multisensory functions. In contrast, the extent to which a transient period of congenital visual deprivation impacts brain structure has not yet been investigated. The present study investigated this by assessing cortical thickness of occipital areas in a group of six cataract-reversal individuals and a group of six age-matched normally sighted controls. This analysis revealed higher cortical thickness in cataract-reversal individuals in the left calcarine sulcus, in the superior occipital gyrus and in the transverse occipital sulcus bilaterally. In addition, occipital cortical thickness correlated negatively with behavioral performance in an audio-visual task for which visual input was critical, and positively with behavioral performance in auditory tasks. Together, these results underscore the critical role of early sensory experience in shaping brain structure and suggest that increased occipital cortical thickness, while potentially compensatory for auditory sensory processing, might be maladaptive for visual recovery in cases of sight restoration.

The effect of early visual deprivation on the neural bases of multisensory processing.

Developmental vision is deemed to be necessary for the maturation of multisensory cortical circuits. Thus far, this has only been investigated in animal studies, which have shown that congenital visual deprivation markedly reduces the capability of neurons to integrate cross-modal inputs. The present study investigated the effect of transient congenital visual deprivation on the neural mechanisms of multisensory processing in humans. We used functional magnetic resonance imaging to compare responses of visual and auditory cortical areas to visual, auditory and audio-visual stimulation in cataract-reversal patients and normally sighted controls. The results showed that cataract-reversal patients, unlike normally sighted controls, did not exhibit multisensory integration in auditory areas. Furthermore, cataract-reversal patients, but not normally sighted controls, exhibited lower visual cortical processing within visual cortex during audio-visual stimulation than during visual stimulation. These results indicate that congenital visual deprivation affects the capability of cortical areas to integrate cross-modal inputs in humans, possibly because visual processing is suppressed during cross-modal stimulation. Arguably, the lack of vision in the first months after birth may result in a reorganization of visual cortex, including the suppression of noisy visual input from the deprived retina in order to reduce interference during auditory processing.

Top-down modulation of visual and auditory cortical processing in aging.

Age-related cognitive decline has been accounted for by an age-related deficit in top-down attentional modulation of sensory cortical processing. In light of recent behavioral findings showing that age-related differences in selective attention are modality dependent, our goal was to investigate the role of sensory modality in age-related differences in top-down modulation of sensory cortical processing. This question was addressed by testing younger and older individuals in several memory tasks while undergoing fMRI. Throughout these tasks, perceptual features were kept constant while attentional instructions were varied, allowing us to devise all combinations of relevant and irrelevant, visual and auditory information. We found no top-down modulation of auditory sensory cortical processing in either age group. In contrast, we found top-down modulation of visual cortical processing in both age groups, and this effect did not differ between age groups. That is, older adults enhanced cortical processing of relevant visual information and suppressed cortical processing of visual distractors during auditory attention to the same extent as younger adults. The present results indicate that older adults are capable of suppressing irrelevant visual information in the context of cross-modal auditory attention, and thereby challenge the view that age-related attentional and cognitive decline is due to a general deficits in the ability to suppress irrelevant information.

Age-equivalent top-down modulation during cross-modal selective attention.

Selective attention involves top-down modulation of sensory cortical areas, such that responses to relevant information are enhanced whereas responses to irrelevant information are suppressed. Suppression of irrelevant information, unlike enhancement of relevant information, has been shown to be deficient in aging. Although these attentional mechanisms have been well characterized within the visual modality, little is known about these mechanisms when attention is selectively allocated across sensory modalities. The present EEG study addressed this issue by testing younger and older participants in three different tasks: Participants attended to the visual modality and ignored the auditory modality, attended to the auditory modality and ignored the visual modality, or passively perceived information presented through either modality. We found overall modulation of visual and auditory processing during cross-modal selective attention in both age groups. Top-down modulation of visual processing was observed as a trend toward enhancement of visual information in the setting of auditory distraction, but no significant suppression of visual distraction when auditory information was relevant. Top-down modulation of auditory processing, on the other hand, was observed as suppression of auditory distraction when visual stimuli were relevant, but no significant enhancement of auditory information in the setting of visual distraction. In addition, greater visual enhancement was associated with better recognition of relevant visual information, and greater auditory distractor suppression was associated with a better ability to ignore auditory distraction. There were no age differences in these effects, suggesting that when relevant and irrelevant information are presented through different sensory modalities, selective attention remains intact in older age.

Aging and response interference across sensory modalities.

Advancing age is associated with decrements in selective attention. It was recently hypothesized that age-related differences in selective attention depend on sensory modality. The goal of the present study was to investigate the role of sensory modality in age-related vulnerability to distraction, using a response interference task. To this end, 16 younger (mean age = 23.1 years) and 24 older (mean age = 65.3 years) adults performed four response interference tasks, involving all combinations of visual and auditory targets and distractors. The results showed that response interference effects differ across sensory modalities, but not across age groups. These results indicate that sensory modality plays an important role in vulnerability to distraction, but not in age-related distractibility by irrelevant spatial information.

Making sense of age-related distractibility: the critical role of sensory modality.

Older adults are known to have reduced inhibitory control and therefore to be more distractible than young adults. Recently, we have proposed that sensory modality plays a crucial role in age-related distractibility. In this study, we examined age differences in vulnerability to unimodal and cross-modal visual and auditory distraction. A group of 24 younger (mean age=21.7 years) and 22 older adults (mean age=65.4 years) performed visual and auditory n-back tasks while ignoring visual and auditory distraction. Whereas reaction time data indicated that both young and older adults are particularly affected by unimodal distraction, accuracy data revealed that older adults, but not younger adults, are vulnerable to cross-modal visual distraction. These results support the notion that age-related distractibility is modality dependent.

Automatic selective attention as a function of sensory modality in aging.

OBJECTIVES: It was recently hypothesized that age-related differences in selective attention depend on sensory modality (Guerreiro, M. J. S., Murphy, D. R., & Van Gerven, P. W. M. (2010). The role of sensory modality in age-related distraction: A critical review and a renewed view. Psychological Bulletin, 136, 975-1022. doi:10.1037/a0020731). So far, this hypothesis has not been tested in automatic selective attention. The current study addressed this issue by investigating age-related differences in automatic spatial cueing effects (i.e., facilitation and inhibition of return [IOR]) across sensory modalities. METHODS: Thirty younger (mean age = 22.4 years) and 25 older adults (mean age = 68.8 years) performed 4 left-right target localization tasks, involving all combinations of visual and auditory cues and targets. We used stimulus onset asynchronies (SOAs) of 100, 500, 1,000, and 1,500 ms between cue and target. RESULTS: The results showed facilitation (shorter reaction times with valid relative to invalid cues at shorter SOAs) in the unimodal auditory and in both cross-modal tasks but not in the unimodal visual task. In contrast, there was IOR (longer reaction times with valid relative to invalid cues at longer SOAs) in both unimodal tasks but not in either of the cross-modal tasks. Most important, these spatial cueing effects were independent of age. DISCUSSION: The results suggest that the modality hypothesis of age-related differences in selective attention does not extend into the realm of automatic selective attention.