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Music-induced cortical plasticity and lateral inhibition in the human auditory cortex as foundations for tonal tinnitus treatment  [PDF]
Christo Pantev,Hidehiko Okamoto,Henning Teismann
Frontiers in Systems Neuroscience , 2012, DOI: 10.3389/fnsys.2012.00050
Abstract: Over the past 15 years, we have studied plasticity in the human auditory cortex by means of magnetoencephalography (MEG). Two main topics nurtured our curiosity: the effects of musical training on plasticity in the auditory system, and the effects of lateral inhibition. One of our plasticity studies found that listening to notched music for 3 h inhibited the neuronal activity in the auditory cortex that corresponded to the center-frequency of the notch, suggesting suppression of neural activity by lateral inhibition. Subsequent research on this topic found that suppression was notably dependent upon the notch width employed, that the lower notch-edge induced stronger attenuation of neural activity than the higher notch-edge, and that auditory focused attention strengthened the inhibitory networks. Crucially, the overall effects of lateral inhibition on human auditory cortical activity were stronger than the habituation effects. Based on these results we developed a novel treatment strategy for tonal tinnitus—tailor-made notched music training (TMNMT). By notching the music energy spectrum around the individual tinnitus frequency, we intended to attract lateral inhibition to auditory neurons involved in tinnitus perception. So far, the training strategy has been evaluated in two studies. The results of the initial long-term controlled study (12 months) supported the validity of the treatment concept: subjective tinnitus loudness and annoyance were significantly reduced after TMNMT but not when notching spared the tinnitus frequencies. Correspondingly, tinnitus-related auditory evoked fields (AEFs) were significantly reduced after training. The subsequent short-term (5 days) training study indicated that training was more effective in the case of tinnitus frequencies ≤ 8 kHz compared to tinnitus frequencies >8 kHz, and that training should be employed over a long-term in order to induce more persistent effects. Further development and evaluation of TMNMT therapy are planned. A goal is to transfer this novel, completely non-invasive and low-cost treatment approach for tonal tinnitus into routine clinical practice.
Cortical GABAergic Interneurons in Cross-Modal Plasticity following Early Blindness  [PDF]
Sébastien Desgent,Maurice Ptito
Neural Plasticity , 2012, DOI: 10.1155/2012/590725
Abstract: Early loss of a given sensory input in mammals causes anatomical and functional modifications in the brain via a process called cross-modal plasticity. In the past four decades, several animal models have illuminated our understanding of the biological substrates involved in cross-modal plasticity. Progressively, studies are now starting to emphasise on cell-specific mechanisms that may be responsible for this intermodal sensory plasticity. Inhibitory interneurons expressing γ-aminobutyric acid (GABA) play an important role in maintaining the appropriate dynamic range of cortical excitation, in critical periods of developmental plasticity, in receptive field refinement, and in treatment of sensory information reaching the cerebral cortex. The diverse interneuron population is very sensitive to sensory experience during development. GABAergic neurons are therefore well suited to act as a gate for mediating cross-modal plasticity. This paper attempts to highlight the links between early sensory deprivation, cortical GABAergic interneuron alterations, and cross-modal plasticity, discuss its implications, and further provide insights for future research in the field. 1. Introduction Patterns of activity from the peripheral sensory receptor arrays can dramatically influence the development of connectivity and functional organization of cortical fields in mammals. In some species, evolution in relation to specific environmental cues has nurtured the brain’s blueprint in such a way that a sensory cortex processing specific survival needs has been enlarged over time as compared to other modalities (Figure 1) [1–5]. Similarly, when a sensory function is lost during development, spared senses compensate by taking more cortical space and recruiting the deafferented areas, to maintain homeostasis of sensory function. This reorganization optimizes and secures the individual’s survival and awareness to future environmental changes. For example, the loss of sight at birth or during early life in humans leads to important anatomical and functional reorganization of the visually deprived cortex that will become activated by a wide variety of nonvisual stimuli involving touch, audition, and olfaction [6–11]. Enhanced spatiotemporal functions in the remaining sensory modalities have also been reported [12–16]. It seems therefore that the visual cortex of the blind is not lifeless and is capable of adapting in order to accommodate these nonvisual inputs through cross-modal plasticity. Figure 1: Primary cortical areas in three species of mammals (i.e., Mouse, Ghost Bat and
Loss of Prestin Does Not Alter the Development of Auditory Cortical Dendritic Spines  [PDF]
L. J. Bogart,A. D. Levy,M. Gladstone,P. D. Allen,M. Zettel,J. R. Ison,A. E. Luebke,A. K. Majewska
Neural Plasticity , 2011, DOI: 10.1155/2011/305621
Abstract: Disturbance of sensory input during development can have disastrous effects on the development of sensory cortical areas. To examine how moderate perturbations of hearing can impact the development of primary auditory cortex, we examined markers of excitatory synapses in mice who lacked prestin, a protein responsible for somatic electromotility of cochlear outer hair cells. While auditory brain stem responses of these mice show an approximately 40?dB increase in threshold, we found that loss of prestin produced no changes in spine density or morphological characteristics on apical dendrites of cortical layer 5 pyramidal neurons. PSD-95 immunostaining also showed no changes in overall excitatory synapse density. Surprisingly, behavioral assessments of auditory function using the acoustic startle response showed only modest changes in prestin KO animals. These results suggest that moderate developmental hearing deficits produce minor changes in the excitatory connectivity of layer 5 neurons of primary auditory cortex and surprisingly mild auditory behavioral deficits in the startle response. 1. Introduction Early loss of sensory input can have profound effects on the development of sensory cortical areas. Early loss of vision has been shown to affect the development of both inhibitory and excitatory neurons in the visual cortex [1], and trimming of whiskers has similar effects on neurons in somatosensory barrel cortex [2]. While less extensively studied, developmental hearing loss has been shown to induce numerous changes in the response properties of auditory cortical neurons [3]. Sensorineural hearing loss in early postnatal life results in enhanced excitability and weakened inhibition in auditory cortex [4, 5]. Interestingly, even conductive hearing loss, which is a relatively mild deprivation of auditory experience, has similar effects on cortical auditory neurons [6]. In visual and somatosensory cortex, excitatory synapses have been shown to be sensitive to sensory manipulation. Manipulations of activity result in changes in the structure and dynamics of dendritic spines [7–11]. These structures are the postsynaptic sites of excitatory connections in the nervous system [12], making them likely substrates for structural plasticity. The shape of dendritic spines has long been thought to have important functional implications [13], and recent experiments have shown that the unique morphology of spines may allow them to compartmentalize calcium and implement synapse-specific plasticity. Thus the detailed morphology of dendritic spines is likely to be
Cortical Auditory Deafferentation Induces Long-Term Plasticity in the Inferior Colliculus of Adult Rats: Microarray and qPCR Analysis  [PDF]
Cheryl Clarkson,M. Javier Herrero-Turrión,Miguel A. Merchán
Frontiers in Neural Circuits , 2012, DOI: 10.3389/fncir.2012.00086
Abstract: The cortico-collicular pathway is a bilateral excitatory projection from the cortex to the inferior colliculus (IC). It is asymmetric and predominantly ipsilateral. Using microarrays and RT-qPCR we analyzed changes in gene expression in the IC after unilateral lesions of the auditory cortex, comparing the ICs ipsi- and contralateral to the lesioned side. At 15 days after surgery there were mainly changes in gene expression in the IC ipsilateral to the lesion. Regulation primarily involved inflammatory cascade genes, suggesting a direct effect of degeneration rather than a neuronal plastic reorganization. Ninety days after the cortical lesion the ipsilateral IC showed a significant up-regulation of genes involved in apoptosis and axonal regeneration combined with a down-regulation of genes involved in neurotransmission, synaptic growth, and gap junction assembly. In contrast, the contralateral IC at 90 days post-lesion showed an up-regulation in genes primarily related to neurotransmission, cell proliferation, and synaptic growth. There was also a down-regulation in autophagy and neuroprotection genes. These findings suggest that the reorganization in the IC after descending pathway deafferentation is a long-term process involving extensive changes in gene expression regulation. Regulated genes are involved in many different neuronal functions, and the number and gene rearrangement profile seems to depend on the density of loss of the auditory cortical inputs.
Multivoxel Pattern Analysis Reveals Auditory Motion Information in MT+ of Both Congenitally Blind and Sighted Individuals  [PDF]
Lukas Strnad, Marius V. Peelen, Marina Bedny, Alfonso Caramazza
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0063198
Abstract: Cross-modal plasticity refers to the recruitment of cortical regions involved in the processing of one modality (e.g. vision) for processing other modalities (e.g. audition). The principles determining how and where cross-modal plasticity occurs remain poorly understood. Here, we investigate these principles by testing responses to auditory motion in visual motion area MT+ of congenitally blind and sighted individuals. Replicating previous reports, we find that MT+ as a whole shows a strong and selective responses to auditory motion in congenitally blind but not sighted individuals, suggesting that the emergence of this univariate response depends on experience. Importantly, however, multivoxel pattern analyses showed that MT+ contained information about different auditory motion conditions in both blind and sighted individuals. These results were specific to MT+ and not found in early visual cortex. Basic sensitivity to auditory motion in MT+ is thus experience-independent, which may be a basis for the region's strong cross-modal recruitment in congenital blindness.
Manipulation of BDNF Signaling Modifies the Experience-Dependent Plasticity Induced by Pure Tone Exposure during the Critical Period in the Primary Auditory Cortex  [PDF]
Renata Anomal, Etienne de Villers-Sidani, Michael M. Merzenich, Rogerio Panizzutti
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0064208
Abstract: Sensory experience powerfully shapes cortical sensory representations during an early developmental “critical period” of plasticity. In the rat primary auditory cortex (A1), the experience-dependent plasticity is exemplified by significant, long-lasting distortions in frequency representation after mere exposure to repetitive frequencies during the second week of life. In the visual system, the normal unfolding of critical period plasticity is strongly dependent on the elaboration of brain-derived neurotrophic factor (BDNF), which promotes the establishment of inhibition. Here, we tested the hypothesis that BDNF signaling plays a role in the experience-dependent plasticity induced by pure tone exposure during the critical period in the primary auditory cortex. Elvax resin implants filled with either a blocking antibody against BDNF or the BDNF protein were placed on the A1 of rat pups throughout the critical period window. These pups were then exposed to 7 kHz pure tone for 7 consecutive days and their frequency representations were mapped. BDNF blockade completely prevented the shaping of cortical tuning by experience and resulted in poor overall frequency tuning in A1. By contrast, BDNF infusion on the developing A1 amplified the effect of 7 kHz tone exposure compared to control. These results indicate that BDNF signaling participates in the experience-dependent plasticity induced by pure tone exposure during the critical period in A1.
Plasticity of the auditory system: theoretical considerations
Kappel, Vanessa;Moreno, Ana Clara de Paula;Buss, Ceres Helena;
Brazilian Journal of Otorhinolaryngology , 2011, DOI: 10.1590/S1808-86942011000500022
Abstract: auditory plasticity refers to the possibility of anatomical and/or functional changes in the system where transmission of auditory information takes place. the auditory system is often required in communication; it is important to learn how the auditory system reacts to stimuli in order to improve performance in individual communication of subjects with impaired hearing. aim: to review the literature on auditory plasticity and the possibility and ability of plastic responses in the auditory system; also to review the evidence of auditory plasticity. methodology: a review of the brazilian and international literature (journals, books, and graduate studies) was carried out. the medline, scielo, bireme, pubmed, and lilacs data bases were consulted, as well as 24 papers from the 1990s to the present date; each paper was assessed for relevance to the topic. conclusion: the findings showed that the auditory system is able to reorganize itself if there is variation, whether by by reducing, increasing, or conditioning of sound stimuli. this is evidence of plasticity in the auditory system.
Cross-Modal Re-Organization in Adults with Early Stage Hearing Loss  [PDF]
Julia Campbell, Anu Sharma
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0090594
Abstract: Cortical cross-modal re-organization, or recruitment of auditory cortical areas for visual processing, has been well-documented in deafness. However, the degree of sensory deprivation necessary to induce such cortical plasticity remains unclear. We recorded visual evoked potentials (VEP) using high-density electroencephalography in nine persons with adult-onset mild-moderate hearing loss and eight normal hearing control subjects. Behavioral auditory performance was quantified using a clinical measure of speech perception-in-noise. Relative to normal hearing controls, adults with hearing loss showed significantly larger P1, N1, and P2 VEP amplitudes, decreased N1 latency, and a novel positive component (P2’) following the P2 VEP. Current source density reconstruction of VEPs revealed a shift toward ventral stream processing including activation of auditory temporal cortex in hearing-impaired adults. The hearing loss group showed worse than normal speech perception performance in noise, which was strongly correlated with a decrease in the N1 VEP latency. Overall, our findings provide the first evidence that visual cross-modal re-organization not only begins in the early stages of hearing impairment, but may also be an important factor in determining behavioral outcomes for listeners with hearing loss, a finding which demands further investigation.
Auditory Cortical Detection and Discrimination Correlates with Communicative Significance  [PDF]
Robert C. Liu,Christoph E. Schreiner
PLOS Biology , 2012, DOI: 10.1371/journal.pbio.0050173
Abstract: Plasticity studies suggest that behavioral relevance can change the cortical processing of trained or conditioned sensory stimuli. However, whether this occurs in the context of natural communication, where stimulus significance is acquired through social interaction, has not been well investigated, perhaps because neural responses to species-specific vocalizations can be difficult to interpret within a systematic framework. The ultrasonic communication system between isolated mouse pups and adult females that either do or do not recognize the calls' significance provides an opportunity to explore this issue. We applied an information-based analysis to multi- and single unit data collected from anesthetized mothers and pup-na?ve females to quantify how the communicative significance of pup calls affects their encoding in the auditory cortex. The timing and magnitude of information that cortical responses convey (at a 2-ms resolution) for pup call detection and discrimination was significantly improved in mothers compared to na?ve females, most likely because of changes in call frequency encoding. This was not the case for a non-natural sound ensemble outside the mouse vocalization repertoire. The results demonstrate that a sensory cortical change in the timing code for communication sounds is correlated with the vocalizations' behavioral relevance, potentially enhancing functional processing by improving its signal to noise ratio.
Auditory Cortical Detection and Discrimination Correlates with Communicative Significance  [PDF]
Robert C Liu ,Christoph E Schreiner
PLOS Biology , 2007, DOI: 10.1371/journal.pbio.0050173
Abstract: Plasticity studies suggest that behavioral relevance can change the cortical processing of trained or conditioned sensory stimuli. However, whether this occurs in the context of natural communication, where stimulus significance is acquired through social interaction, has not been well investigated, perhaps because neural responses to species-specific vocalizations can be difficult to interpret within a systematic framework. The ultrasonic communication system between isolated mouse pups and adult females that either do or do not recognize the calls' significance provides an opportunity to explore this issue. We applied an information-based analysis to multi- and single unit data collected from anesthetized mothers and pup-na?ve females to quantify how the communicative significance of pup calls affects their encoding in the auditory cortex. The timing and magnitude of information that cortical responses convey (at a 2-ms resolution) for pup call detection and discrimination was significantly improved in mothers compared to na?ve females, most likely because of changes in call frequency encoding. This was not the case for a non-natural sound ensemble outside the mouse vocalization repertoire. The results demonstrate that a sensory cortical change in the timing code for communication sounds is correlated with the vocalizations' behavioral relevance, potentially enhancing functional processing by improving its signal to noise ratio.
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