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Neural circuits underlying adaptation and learning in the perception of auditory space.

King AJ, Dahmen JC, Keating P, Leach ND, Nodal FR, Bajo VM - Neurosci Biobehav Rev (2011)

Bottom Line: Sound localization mechanisms are particularly plastic during development, when the monaural and binaural acoustic cues that form the basis for spatial hearing change in value as the body grows.Recent studies have shown that the mature brain retains a surprising capacity to relearn to localize sound in the presence of substantially altered auditory spatial cues.Through a combination of recording studies and methods for selectively manipulating the activity of specific neuronal populations, progress is now being made in identifying the cortical and subcortical circuits in the brain that are responsible for the dynamic coding of auditory spatial information.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Genetics, Sherrington Building, University of Oxford, Parks Road, Oxford, UK. andrew.king@dpag.ox.ac.uk

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The auditory corticocollicular projection is required for training-induced plasticity of spatial hearing. (A) Layer V corticocollicular pyramidal cells were retrogradely labeled by making injections into the inferior colliculus of fluorescent microspheres coated with a specific chromophore. Apoptosis was selectively triggered in the labeled neurons by applying near-infrared light (λ = 670 nm) to the primary auditory cortex in the middle ectosylvian gyrus. (B) The loss of corticocollicular neurons in the left auditory cortex is indicated by expressing the number of labeled neurons on that side as a percentage of those in the right hemisphere, contralateral to the injection sites in the inferior colliculus. This ipsilateral/contralateral ratio is about 15–20% in control cases, but much larger following chromophore-targeted laser photolysis, indicating a substantial loss of labeled cells in the targeted auditory cortex (**P < 0.01). (C) Sound localization accuracy in the horizontal plane was unchanged even when very brief sound durations were used, with no differences between the ferrets with corticocollicular lesions and controls. The lines depict the mean values for the lesioned cases at two different sound durations, 1000 ms in black and 40 ms in gray, and the gray bands correspond to 1 s.d. on either side of the mean values achieved by control ferrets. (D) The ability to adapt to altered spatial cues caused by the monaural insertion of an earplug was impaired in ferrets with corticocollicular lesions (black), with no improvement observed with training compared with control cases (gray). The lines are mean values for each group. Abbreviations: AEG, anterior ectosylvian gyrus; IC, inferior colliculus; MEG, middle ectosylvian gyrus; PEG, posterior ectosylvian gyrus.
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fig0020: The auditory corticocollicular projection is required for training-induced plasticity of spatial hearing. (A) Layer V corticocollicular pyramidal cells were retrogradely labeled by making injections into the inferior colliculus of fluorescent microspheres coated with a specific chromophore. Apoptosis was selectively triggered in the labeled neurons by applying near-infrared light (λ = 670 nm) to the primary auditory cortex in the middle ectosylvian gyrus. (B) The loss of corticocollicular neurons in the left auditory cortex is indicated by expressing the number of labeled neurons on that side as a percentage of those in the right hemisphere, contralateral to the injection sites in the inferior colliculus. This ipsilateral/contralateral ratio is about 15–20% in control cases, but much larger following chromophore-targeted laser photolysis, indicating a substantial loss of labeled cells in the targeted auditory cortex (**P < 0.01). (C) Sound localization accuracy in the horizontal plane was unchanged even when very brief sound durations were used, with no differences between the ferrets with corticocollicular lesions and controls. The lines depict the mean values for the lesioned cases at two different sound durations, 1000 ms in black and 40 ms in gray, and the gray bands correspond to 1 s.d. on either side of the mean values achieved by control ferrets. (D) The ability to adapt to altered spatial cues caused by the monaural insertion of an earplug was impaired in ferrets with corticocollicular lesions (black), with no improvement observed with training compared with control cases (gray). The lines are mean values for each group. Abbreviations: AEG, anterior ectosylvian gyrus; IC, inferior colliculus; MEG, middle ectosylvian gyrus; PEG, posterior ectosylvian gyrus.

Mentions: Another issue concerning the role of different auditory cortical fields in sound localization and its recalibration by experience is the involvement of neurons located in different cortical layers. A recent study showed that auditory spatial learning is critically dependent on the descending projection from A1 to the auditory midbrain (Bajo et al., 2010; Fig. 4). To demonstrate this, cortical layer V pyramidal cells were first retrogradely labeled by injecting fluorescent microbeads conjugated with chlorine e6 in the left IC, and subsequently killed by illuminating the ipsilateral auditory cortex with near-infrared light (Fig. 4A). The ratio of crossed to uncrossed corticocollicular projection neurons is normally about 20%, and on the basis of the threefold increase in this ratio, Bajo et al. (2010) estimated that chromophore-targeted laser photolysis removed about two thirds of the A1 neurons that project to the IC, without affecting those in surrounding cortical areas (Fig. 4B). No change in sound localization accuracy was observed, even at short stimulus sound durations (Fig. 4C), indicating that loss of the majority of layer V corticocollicular neurons does not result in the same localization deficits that are produced by complete aspiration lesions of A1. However, the spatial plasticity that normally occurs after altering the interaural balance by plugging one ear was severely impaired (Fig. 4D), suggesting that corticofugal pathways are essential for recalibration of the brain's representation of auditory space.


Neural circuits underlying adaptation and learning in the perception of auditory space.

King AJ, Dahmen JC, Keating P, Leach ND, Nodal FR, Bajo VM - Neurosci Biobehav Rev (2011)

The auditory corticocollicular projection is required for training-induced plasticity of spatial hearing. (A) Layer V corticocollicular pyramidal cells were retrogradely labeled by making injections into the inferior colliculus of fluorescent microspheres coated with a specific chromophore. Apoptosis was selectively triggered in the labeled neurons by applying near-infrared light (λ = 670 nm) to the primary auditory cortex in the middle ectosylvian gyrus. (B) The loss of corticocollicular neurons in the left auditory cortex is indicated by expressing the number of labeled neurons on that side as a percentage of those in the right hemisphere, contralateral to the injection sites in the inferior colliculus. This ipsilateral/contralateral ratio is about 15–20% in control cases, but much larger following chromophore-targeted laser photolysis, indicating a substantial loss of labeled cells in the targeted auditory cortex (**P < 0.01). (C) Sound localization accuracy in the horizontal plane was unchanged even when very brief sound durations were used, with no differences between the ferrets with corticocollicular lesions and controls. The lines depict the mean values for the lesioned cases at two different sound durations, 1000 ms in black and 40 ms in gray, and the gray bands correspond to 1 s.d. on either side of the mean values achieved by control ferrets. (D) The ability to adapt to altered spatial cues caused by the monaural insertion of an earplug was impaired in ferrets with corticocollicular lesions (black), with no improvement observed with training compared with control cases (gray). The lines are mean values for each group. Abbreviations: AEG, anterior ectosylvian gyrus; IC, inferior colliculus; MEG, middle ectosylvian gyrus; PEG, posterior ectosylvian gyrus.
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fig0020: The auditory corticocollicular projection is required for training-induced plasticity of spatial hearing. (A) Layer V corticocollicular pyramidal cells were retrogradely labeled by making injections into the inferior colliculus of fluorescent microspheres coated with a specific chromophore. Apoptosis was selectively triggered in the labeled neurons by applying near-infrared light (λ = 670 nm) to the primary auditory cortex in the middle ectosylvian gyrus. (B) The loss of corticocollicular neurons in the left auditory cortex is indicated by expressing the number of labeled neurons on that side as a percentage of those in the right hemisphere, contralateral to the injection sites in the inferior colliculus. This ipsilateral/contralateral ratio is about 15–20% in control cases, but much larger following chromophore-targeted laser photolysis, indicating a substantial loss of labeled cells in the targeted auditory cortex (**P < 0.01). (C) Sound localization accuracy in the horizontal plane was unchanged even when very brief sound durations were used, with no differences between the ferrets with corticocollicular lesions and controls. The lines depict the mean values for the lesioned cases at two different sound durations, 1000 ms in black and 40 ms in gray, and the gray bands correspond to 1 s.d. on either side of the mean values achieved by control ferrets. (D) The ability to adapt to altered spatial cues caused by the monaural insertion of an earplug was impaired in ferrets with corticocollicular lesions (black), with no improvement observed with training compared with control cases (gray). The lines are mean values for each group. Abbreviations: AEG, anterior ectosylvian gyrus; IC, inferior colliculus; MEG, middle ectosylvian gyrus; PEG, posterior ectosylvian gyrus.
Mentions: Another issue concerning the role of different auditory cortical fields in sound localization and its recalibration by experience is the involvement of neurons located in different cortical layers. A recent study showed that auditory spatial learning is critically dependent on the descending projection from A1 to the auditory midbrain (Bajo et al., 2010; Fig. 4). To demonstrate this, cortical layer V pyramidal cells were first retrogradely labeled by injecting fluorescent microbeads conjugated with chlorine e6 in the left IC, and subsequently killed by illuminating the ipsilateral auditory cortex with near-infrared light (Fig. 4A). The ratio of crossed to uncrossed corticocollicular projection neurons is normally about 20%, and on the basis of the threefold increase in this ratio, Bajo et al. (2010) estimated that chromophore-targeted laser photolysis removed about two thirds of the A1 neurons that project to the IC, without affecting those in surrounding cortical areas (Fig. 4B). No change in sound localization accuracy was observed, even at short stimulus sound durations (Fig. 4C), indicating that loss of the majority of layer V corticocollicular neurons does not result in the same localization deficits that are produced by complete aspiration lesions of A1. However, the spatial plasticity that normally occurs after altering the interaural balance by plugging one ear was severely impaired (Fig. 4D), suggesting that corticofugal pathways are essential for recalibration of the brain's representation of auditory space.

Bottom Line: Sound localization mechanisms are particularly plastic during development, when the monaural and binaural acoustic cues that form the basis for spatial hearing change in value as the body grows.Recent studies have shown that the mature brain retains a surprising capacity to relearn to localize sound in the presence of substantially altered auditory spatial cues.Through a combination of recording studies and methods for selectively manipulating the activity of specific neuronal populations, progress is now being made in identifying the cortical and subcortical circuits in the brain that are responsible for the dynamic coding of auditory spatial information.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Genetics, Sherrington Building, University of Oxford, Parks Road, Oxford, UK. andrew.king@dpag.ox.ac.uk

Show MeSH
Related in: MedlinePlus