Cross-modal Reorganization Research Articles

Early Hearing-Impairment Results in Crossmodal Reorganization of Ferret Core Auditory Cortex

Numerous investigations of cortical crossmodal plasticity, most often in congenital or early-deaf subjects, have indicated that secondary auditory cortical areas reorganize to exhibit visual responsiveness while the core auditory regions are largely spared. However, a recent study of adult-deafened ferrets demonstrated that core auditory cortex was reorganized by the somatosensory modality. Because adult animals have matured beyond their critical period of sensory development and plasticity, it was not known if adult-deafening and early-deafening would generate the same crossmodal results. The present study used young, ototoxically-lesioned ferrets (n = 3) that, after maturation (avg. = 173 days old), showed significant hearing deficits (avg. threshold = 72 dB SPL). Recordings from single-units (n = 132) in core auditory cortex showed that 72% were activated by somatosensory stimulation (compared to 1% in hearing controls). In addition, tracer injection into early hearing-impaired core auditory cortex labeled essentially the same auditory cortical and thalamic projection sources as seen for injections in the hearing controls, indicating that the functional reorganization was not the result of new or latent projections to the cortex. These data, along with similar observations from adult-deafened and adult hearing-impaired animals, support the recently proposed brainstem theory for crossmodal plasticity induced by hearing loss.

Cortical thickness analysis and optimized voxel-based morphometry in children and adolescents with prelingually profound sensorineural hearing loss

Crossmodal neuroplastic changes following auditory deprivation in individuals with profound sensorineural hearing loss (SNHL) have been well documented in previous literature. However, previous studies have shown very little evidence of structural brain changes in individuals with prelingually profound SNHL and no studies have reported significant differences of gray matter (GM) in deaf subjects. Therefore, it is essential to employ a more specific and sensitive technique to detect subtle structural brain differences in deaf individuals. The objective of our study was to investigate neuroanatomical differences in children and adolescents with profound SNHL by cortical thickness analysis and optimized voxel-based morphometry (VBM). T1-weighted volumetric images of 16 children and adolescents with prelingually profound SNHL and 16 hearing controls were analyzed. The ANCOVA analysis revealed a statistically significant decreased average cortical thickness of the whole brain. As to vertex-based analysis, cortical thickness of the deaf subjects showed significant thinning in the left precentral gyrus, right postcentral gyrus, the left superior occipital gyrus and the left fusiform gyrus compared with the hearing subjects. VBM revealed statistically significant focal reduction of white matter (WM) volume in the left middle frontal gyrus and the right inferior occipital gyrus in deaf subjects without statistically significant differences in GM volume between the two groups. These findings demonstrated that structural changes happened not only in the WM but also in the GM of the subjects with prelingually profound SNHL, which have never been reported before in any previous literature. Our results also implicated the potential neuroplastic changes associated with crossmodal reorganization in the brain after auditory deprivation in the early deafness.

Serotonin mediates cross-modal reorganization of cortical circuits

Serotonin mediates cross-modal reorganization of cortical circuits

Serotonin as a mediator of cross-modal cortical reorganization

When one type of sensory system is disrupted, other intact remaining sensory function can be improved. Although this form of plasticity, cross-modal plasticity, is widely known, the molecular and cellular mechanisms underlying it are poorly understood. In a recent study, we demonstrated that visual deprivation increases extracellular serotonin in the juvenile rat barrel cortex and resulted in facilitation of synaptic delivery of AMPA-type glutamate receptors (AMPARs) at layer4-2/3 synapses in the barrel cortex via the activation of serotonin 5HT2A/2C receptors and ERK. This caused sharpening of functional whisker-barrel map at layer2/3 of the barrel cortex. Thus, sensory dysfunction of one modality leads to improvement of remaining modalities by the refinement of cortical organization through serotonin signaling-mediated facilitation of synaptic AMPARs delivery.

Serotonin as a mediator of cross-modal cortical reorganization.

When one type of sensory system is disrupted, other intact remaining sensory function can be improved. Although this form of plasticity, cross-modal plasticity, is widely known, the molecular and cellular mechanisms underlying it are poorly understood. In a recent study, we demonstrated that visual deprivation increases extracellular serotonin in the juvenile rat barrel cortex and resulted in facilitation of synaptic delivery of AMPA-type glutamate receptors (AMPARs) at layer4-2/3 synapses in the barrel cortex via the activation of serotonin 5HT2A/2C receptors and ERK. This caused sharpening of functional whisker-barrel map at layer2/3 of the barrel cortex. Thus, sensory dysfunction of one modality leads to improvement of remaining modalities by the refinement of cortical organization through serotonin signaling-mediated facilitation of synaptic AMPARs delivery.

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex.

It is well known that early disruption of sensory input from one modality can induce crossmodal reorganization of a deprived cortical area, resulting in compensatory abilities in the remaining senses. Compensatory effects, however, occur in selected cortical regions and it is not known whether such compensatory phenomena have any relation to the original function of the reorganized area. In the cortex of hearing cats, the auditory field of the anterior ectosylvian sulcus (FAES) is largely responsive to acoustic stimulation and its unilateral deactivation results in profound contralateral acoustic orienting deficits. Given these functional and behavioral roles, the FAES was studied in early-deafened cats to examine its crossmodal sensory properties as well as to assess the behavioral role of that reorganization. Recordings in the FAES of early-deafened adults revealed robust responses to visual stimulation as well as receptive fields that collectively represented the contralateral visual field. A second group of early-deafened cats was trained to localize visual targets in a perimetry array. In these animals, cooling loops were surgically placed on the FAES to reversibly deactivate the region, which resulted in substantial contralateral visual orienting deficits. These results demonstrate that crossmodal plasticity can substitute one sensory modality for another while maintaining the functional repertoire of the reorganized region.

Evolution of crossmodal reorganization of the voice area in cochlear‐implanted deaf patients

Psychophysical and neuroimaging studies in both animal and human subjects have clearly demonstrated that cortical plasticity following sensory deprivation leads to a brain functional reorganization that favors the spared modalities. In postlingually deaf patients, the use of a cochlear implant (CI) allows a recovery of the auditory function, which will probably counteract the cortical crossmodal reorganization induced by hearing loss. To study the dynamics of such reversed crossmodal plasticity, we designed a longitudinal neuroimaging study involving the follow-up of 10 postlingually deaf adult CI users engaged in a visual speechreading task. While speechreading activates Broca's area in normally hearing subjects (NHS), the activity level elicited in this region in CI patients is abnormally low and increases progressively with post-implantation time. Furthermore, speechreading in CI patients induces abnormal crossmodal activations in right anterior regions of the superior temporal cortex normally devoted to processing human voice stimuli (temporal voice-sensitive areas-TVA). These abnormal activity levels diminish with post-implantation time and tend towards the levels observed in NHS. First, our study revealed that the neuroplasticity after cochlear implantation involves not only auditory but also visual and audiovisual speech processing networks. Second, our results suggest that during deafness, the functional links between cortical regions specialized in face and voice processing are reallocated to support speech-related visual processing through cross-modal reorganization. Such reorganization allows a more efficient audiovisual integration of speech after cochlear implantation. These compensatory sensory strategies are later completed by the progressive restoration of the visuo-audio-motor speech processing loop, including Broca's area.

Functional selectivity in sensory-deprived cortices

In a recent study, Lomber, Meredith, and Kral (2010) investigated crossmodal reorganization in congenitally deaf cats. They demonstrated that specific regions of the auditory cortex are responsible for distinct supranormal visual performances following early auditory deprivation. These exciting results are considered in light of recently increasing research suggesting that crossmodal plasticity associated with early sensory deprivation follows organizational principles that maintain the functional specialization of the colonized brain regions.

Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats

It is well known that the post-natal loss of sensory input in one modality can result in crossmodal reorganization of the deprived cortical areas, but deafness fails to induce crossmodal effects in cat primary auditory cortex (A1). Because the core auditory regions (A1, and anterior auditory field AAF) are arranged as separate, parallel processors, it cannot be assumed that early-deafness affects one in the same manner as the other. The present experiments were conducted to determine if crossmodal effects occur in the anterior auditory field (AAF). Using mature cats (n = 3), ototoxically deafened postnatally, single-unit recordings were made in the gyral and sulcal portions of the AAF. In contrast to the auditory responsivity found in the hearing controls, none of the neurons in early-deafened AAF were activated by auditory stimulation. Instead, the majority (78%) were activated by somatosensory cues, while fewer were driven by visual stimulation (44%; values include unisensory and bimodal neurons). Somatosensory responses could be activated from all locations on the body surface but most often occurred on the head, were often bilateral (e.g., occupied portions of both sides of the body), and were primarily excited by low-threshold hair receptors. Visual receptive fields were large, collectively represented the contralateral visual field, and exhibited conventional response properties such as movement direction and velocity preferences. These results indicate that, following post-natal deafness, both somatosensory and visual modalities participate in crossmodal reinnervation of the AAF, consistent with the growing literature that documents deafness-induced crossmodal plasticity outside A1.

Voice discrimination in cochlear-implanted deaf subjects

The human voice is important for social communication because voices carry speech and other information such as a person’s physical characteristics and affective state. Further restricted temporal cortical regions are specifically involved in voice processing. In cochlear-implanted deaf patients, the processor alters the spectral cues which are crucial for the perception of the paralinguistic information of human voices. The aim of this study was to assess the abilities of voice discrimination in cochlear-implant (CI) users and in normal-hearing subjects (NHS) using a CI simulation (vocoder). In NHS the performance in voice discrimination decreased when reducing the spectral information by decreasing the number of channels of the vocoder. In CI patients with different delays after implantation we observed a strong impairment in voice discrimination at time of activation of the neuroprosthesis. No significant improvement can be detected in patients after two years of experience of the implant while they have reached a higher level of recovery of speech perception, suggesting a dissociation in the dynamic of functional recuperation of speech and voice processing. In addition to the lack of spectral cues due to the implant processor, we hypothesized that the origin of such deficit could derive from a crossmodal reorganization of the temporal voice areas in CI patients.

Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf

When the brain is deprived of input from one sensory modality, it often compensates with supranormal performance in one or more of the intact sensory systems. In the absence of acoustic input, it has been proposed that cross-modal reorganization of deaf auditory cortex may provide the neural substrate mediating compensatory visual function. We tested this hypothesis using a battery of visual psychophysical tasks and found that congenitally deaf cats, compared with hearing cats, have superior localization in the peripheral field and lower visual movement detection thresholds. In the deaf cats, reversible deactivation of posterior auditory cortex selectively eliminated superior visual localization abilities, whereas deactivation of the dorsal auditory cortex eliminated superior visual motion detection. Our results indicate that enhanced visual performance in the deaf is caused by cross-modal reorganization of deaf auditory cortex and it is possible to localize individual visual functions in discrete portions of reorganized auditory cortex.

Verbal memory retrieval engages visual cortex in musicians

As one major line of research on brain plasticity, many imaging studies have been conducted to identify the functional and structural reorganization associated with musical expertise. Based on previous behavioral research, the present study used functional magnetic resonance imaging to identify the neural correlates of superior verbal memory performance in musicians. Participants with and without musical training performed a verbal memory task to first encode a list of words auditorily delivered and then silently recall as many words as possible. They performed in separate blocks a control task involving pure tone pitch judgment. Post-scan recognition test showed better memory performance in musicians than non-musicians. During memory retrieval, the musicians showed significantly greater activations in bilateral though left-lateralized visual cortex relative to the pitch judgment baseline. In comparison, no such visual cortical activations were found in the non-musicians. No group differences were observed during the encoding stage. The results echo a previous report of visual cortical activation during verbal memory retrieval in the absence of any visual sensory stimulation in the blind population, who are also known to possess superior verbal memory. It is suggested that the visual cortex can be recruited to serve as extra memory resources and contributes to the superior verbal memory in special situations. While in the blind population, such cross-modal functional reorganization may be induced by sensory deprivation; in the musicians it may be induced by the long-term and demanding nature of musical training to use as much available neural resources as possible.

Serotonin mediates cross-modal reorganization of cortical circuits

Serotonin mediates cross-modal reorganization of cortical circuits

Attentional enhancements and deficits in deaf populations: An integrative review

The literature on visual attention in deaf individuals presents two competing views. On one hand, the deficit view proposes that auditory input is necessary for the development of visual attention; on the other hand, the compensation view holds that visual attention reorganizes to allow the individual to compensate for the lack of auditory input. While apparently contradictory, we suggest that these views shed complementary light on the cross-modal reorganization of visual attention after early deafness. First, these two fields of inquiry look at different aspects of attention. The deficit view is mostly supported by studies of allocation of attention in time, whereas the compensation view is backed by studies measuring the allocation of attention across space. Second, they focus on groups of different age and different background. Deficits have been documented mostly in children with mixed hearing loss aetiologies, whereas reorganization has been documented in a less representative, but more homogenous group of Deaf adults. We propose a more integrative view in which early auditory deprivation does not result in better or worse visual attention. Rather, selected aspects of visual attention are modified in various ways along the developmental trajectory as a result of early deafness.

Brain regions responsible for the cross-modal reorganization of cortical circuit

Brain regions responsible for the cross-modal reorganization of cortical circuit

Adult deafness induces somatosensory conversion of ferret auditory cortex

In response to early or developmental lesions, responsiveness of sensory cortex can be converted from the deprived modality to that of the remaining sensory systems. However, little is known about capacity of the adult cortex for cross-modal reorganization. The present study examined the auditory cortices of animals deafened as adults, and observed an extensive somatosensory conversion within as little as 16 days after deafening. These results demonstrate that cortical cross-modal reorganization can occur after the period of sensory system maturation.

Cortical development, plasticity and re-organization in children with cochlear implants

A basic tenet of developmental neurobiology is that certain areas of the cortex will re-organize, if appropriate stimulation is withheld for long periods. Stimulation must be delivered to a sensory system within a narrow window of time (a sensitive period) if that system is to develop normally. In this article, we will describe age cut-offs for a sensitive period for central auditory development in children who receive cochlear implants. We will review de-coupling and re-organization of cortical areas, which are presumed to underlie the end of the sensitive period in congenitally deaf humans and cats. Finally, we present two clinical cases which demonstrate the use of the P1 cortical auditory evoked potential as a biomarker for central auditory system development and re-organization in congenitally deaf children fitted with cochlear implants. Learning outcomes: Readers of this article should be able to (i) describe the importance of the sensitive period as it relates to development of central auditory pathways in children with cochlear implants; (ii) discuss the hypothesis of de-coupling of primary from higher-order auditory cortex as it relates to the end of the sensitive period; (iii) discuss cross-modal re-organization which may occur after long periods of auditory deprivation; and (iv) understand the use of the P1 response as a biomarker for development of central auditory pathways.

Retinotopically Specific Reorganization of Visual Cortex for Tactile Pattern Recognition

Although previous studies have shown that Braille reading and other tactile discrimination tasks activate the visual cortex of blind and sighted people, it is not known whether this kind of crossmodal reorganization is influenced by retinotopic organization. We have addressed this question by studying "S," a visually impaired adult with the rare ability to read print visually and Braille by touch. S had normal visual development until 6 years of age, and thereafter severe acuity reduction due to corneal opacification, but no evidence of visual-field loss. Functional magnetic resonance imaging revealed that, in S's early visual areas, tactile information processing activated what would be the foveal representation for normally sighted individuals, and visual information processing activated what would be the peripheral representation. Control experiments showed that this activation pattern was not due to visual imagery. S's high-level visual areas, which correspond to shape- and object-selective areas in normally sighted individuals, were activated by both visual and tactile stimuli. The retinotopically specific reorganization in early visual areas suggests an efficient redistribution of neural resources in the visual cortex.

Serotonin mediates cross modal reorganization of cortical circuit

Serotonin mediates cross modal reorganization of cortical circuit

Cortical plasticity in blind individual

The cognitive mechanisms and functional brain imaging research on blind individuals provide special information for exploring the plasticity of the developing human brain. This paper focuses on five aspects of recent progress in this field: (1) the behavior compensation of the blind; (2) the influence of early visual deprivation and later visual deprivation on cross-modal reorganization; (3) the relationship between the complexity of task requirement and cross-modal reorganization; (4) the relationship between the sensitive periods of the visual system and the time course of cross-modal reorganization; (5) the neural mechanisms of cross-modal reorganization. These findings contribute greatly to the theoretical basis of the rehabilitation of individuals with perceptual deficits.