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Flexibility and Stability in Sensory Processing Revealed Using Visual-to-Auditory Sensory Substitution.

Hertz U, Amedi A - Cereb. Cortex (2014)

Bottom Line: Secondly, associative areas changed their sensory response profile from strongest response for visual to that for auditory.Consistent features were also found in the sensory dominance in sensory areas and audiovisual convergence in associative area Middle Temporal Gyrus.These 2 factors allow for both stability and a fast, dynamic tuning of the system when required.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical Neurobiology, Institute for Medical Research Israel-Canada (IMRIC), Hadassah Medical School, Hebrew University of Jerusalem, Jerusalem 91220, Israel Interdisciplinary Center for Neural Computation, The Edmond & Lily Safra Center for Brain Sciences (ELSC), Hebrew University of Jerusalem, Jerusalem 91905, Israel.

No MeSH data available.


Related in: MedlinePlus

Dynamic crossmodal attenuations of sensory areas. (A) Statistical parametric map of the learning effect revealed by a two-way ANOVA, post-learning versus pre-learning preference (P < 0.05, corr.), is presented on a flattened cortical reconstruction of one of the subjects. The analysis was carried out within areas that were responsive to either vision or auditory inputs, before or after learning SSA. The statistical parametric map revealed a preference for the pre-learning condition within the right visual cortex, and a preference for the post-learning condition within the left auditory cortex. Retinotopic and tonotopic borders are presented as well; blue lines delineate tonotopic areas and red lines delineate retinotopic areas. (B) Beta values sampled from the clusters depicted in (A) reveal that the learning effect stemmed from changes in crossmodal attenuations (grey dots represent single subjects' beta values; means and SD are presented). In primary visual areas (on the left), visual responses were significantly positive throughout the experiments (*P < 0.05, **P < 0.005, ***P < 0.0005, corr.). However, auditory responses were significantly negative during the Post-passive experiment, underlying the learning effect in this area. In the primary auditory cluster, auditory stimuli elicited significant positive responses throughout the experiments, but visual responses were negative in the “Pre” and “Plus” experiments. (C) Auditory responses in the visual cortex (blue box, left) and visual responses in the auditory cortex (red box, right) in all 3 experimental conditions (Pre, Post, and Plus, in left to right panels), compared with baseline. In all cases, only negative responses were detected, if any (P < 0.05, uncorrected). Here, as well tonotopic borders are in blue and retinotopic borders are depicted in red. In the visual cortex, auditory responses were not presented before learning SSA, but appeared both after learning and in the audiovisual integration task. This experimental context-dependent crossmodal effect underlies the preference of the visual cortex for the pre-learning condition. In the auditory cortex, a mirror pattern appeared with visual attenuation before learning and not afterwards. This release of attenuation explains the preference in the auditory cortex for the post-learning. In the Plus experiment, both crossmodal effects were apparent.
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BHU010F3: Dynamic crossmodal attenuations of sensory areas. (A) Statistical parametric map of the learning effect revealed by a two-way ANOVA, post-learning versus pre-learning preference (P < 0.05, corr.), is presented on a flattened cortical reconstruction of one of the subjects. The analysis was carried out within areas that were responsive to either vision or auditory inputs, before or after learning SSA. The statistical parametric map revealed a preference for the pre-learning condition within the right visual cortex, and a preference for the post-learning condition within the left auditory cortex. Retinotopic and tonotopic borders are presented as well; blue lines delineate tonotopic areas and red lines delineate retinotopic areas. (B) Beta values sampled from the clusters depicted in (A) reveal that the learning effect stemmed from changes in crossmodal attenuations (grey dots represent single subjects' beta values; means and SD are presented). In primary visual areas (on the left), visual responses were significantly positive throughout the experiments (*P < 0.05, **P < 0.005, ***P < 0.0005, corr.). However, auditory responses were significantly negative during the Post-passive experiment, underlying the learning effect in this area. In the primary auditory cluster, auditory stimuli elicited significant positive responses throughout the experiments, but visual responses were negative in the “Pre” and “Plus” experiments. (C) Auditory responses in the visual cortex (blue box, left) and visual responses in the auditory cortex (red box, right) in all 3 experimental conditions (Pre, Post, and Plus, in left to right panels), compared with baseline. In all cases, only negative responses were detected, if any (P < 0.05, uncorrected). Here, as well tonotopic borders are in blue and retinotopic borders are depicted in red. In the visual cortex, auditory responses were not presented before learning SSA, but appeared both after learning and in the audiovisual integration task. This experimental context-dependent crossmodal effect underlies the preference of the visual cortex for the pre-learning condition. In the auditory cortex, a mirror pattern appeared with visual attenuation before learning and not afterwards. This release of attenuation explains the preference in the auditory cortex for the post-learning. In the Plus experiment, both crossmodal effects were apparent.

Mentions: We used the ANOVA learning effect to chart the changes in sensory responses following learning (Table 1, learning effect). Post hoc analysis was carried out to examine the direction of the effect, and post-learning conditions (auditory and visual) were compared with the pre-learning conditions (Fig. 3A). The learning effect was examined within areas which were positively responsive to either auditory or visual stimuli. A significant preference for post-learning conditions was found in the right PT (Brodmann 41), and a significant preference for the pre-learning conditions was found in the left Inferior Occipital Gyrus (IOG, Brodmann 19; Fig. 3A, P < 0.05, corr.). The positive cluster in the auditory cortex was located well within the areas responsive to auditory stimuli as defined by the ANOVA modality effect (Fig. 2A, in blue), and was on the border of the tonotopic responsive areas with some of it within and some outside. This indicates that the learning effect was not only in the primary auditory area, but also in the associative auditory areas (Striem-Amit et al. 2011), in line with previous crossmodal effect reports in the auditory cortex (Foxe et al. 2002; Kayser et al. 2008). The visual cluster lay within the retinotopic boundaries in the foveal part of area V3 and LO. To better understand these learning effects, the GLM-evaluated beta values were sampled from these areas (Fig. 3B). Auditory and visual beta values from the 3 experimental conditions (“Pre,” “Post,” and “Plus”) were tested for significant responses, and the results were corrected for multiple comparisons using a false discovery rate (FDR) correction. In the left IOG, positive beta values were found for visual conditions in all 3 experiments. However, the auditory responses were not significantly different from zero before learning and were significantly negative in the “Post” condition. This suggests that the preference for the pre-learning condition found in visual areas was due to the auditory attenuations (as suggested by the negative beta values) in this area after learning the visual-to-auditory SSA. It should be noted that negative beta values do not necessarily mean a negative BOLD signal, but rather attenuations of the positive signal. In this case, visual responses in visual areas were significantly lower, yet still positive, when accompanied by auditory stimuli after SSA learning, compared with times when those were not accompanied by auditory stimuli (see Methods for further details).Figure 3.


Flexibility and Stability in Sensory Processing Revealed Using Visual-to-Auditory Sensory Substitution.

Hertz U, Amedi A - Cereb. Cortex (2014)

Dynamic crossmodal attenuations of sensory areas. (A) Statistical parametric map of the learning effect revealed by a two-way ANOVA, post-learning versus pre-learning preference (P < 0.05, corr.), is presented on a flattened cortical reconstruction of one of the subjects. The analysis was carried out within areas that were responsive to either vision or auditory inputs, before or after learning SSA. The statistical parametric map revealed a preference for the pre-learning condition within the right visual cortex, and a preference for the post-learning condition within the left auditory cortex. Retinotopic and tonotopic borders are presented as well; blue lines delineate tonotopic areas and red lines delineate retinotopic areas. (B) Beta values sampled from the clusters depicted in (A) reveal that the learning effect stemmed from changes in crossmodal attenuations (grey dots represent single subjects' beta values; means and SD are presented). In primary visual areas (on the left), visual responses were significantly positive throughout the experiments (*P < 0.05, **P < 0.005, ***P < 0.0005, corr.). However, auditory responses were significantly negative during the Post-passive experiment, underlying the learning effect in this area. In the primary auditory cluster, auditory stimuli elicited significant positive responses throughout the experiments, but visual responses were negative in the “Pre” and “Plus” experiments. (C) Auditory responses in the visual cortex (blue box, left) and visual responses in the auditory cortex (red box, right) in all 3 experimental conditions (Pre, Post, and Plus, in left to right panels), compared with baseline. In all cases, only negative responses were detected, if any (P < 0.05, uncorrected). Here, as well tonotopic borders are in blue and retinotopic borders are depicted in red. In the visual cortex, auditory responses were not presented before learning SSA, but appeared both after learning and in the audiovisual integration task. This experimental context-dependent crossmodal effect underlies the preference of the visual cortex for the pre-learning condition. In the auditory cortex, a mirror pattern appeared with visual attenuation before learning and not afterwards. This release of attenuation explains the preference in the auditory cortex for the post-learning. In the Plus experiment, both crossmodal effects were apparent.
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BHU010F3: Dynamic crossmodal attenuations of sensory areas. (A) Statistical parametric map of the learning effect revealed by a two-way ANOVA, post-learning versus pre-learning preference (P < 0.05, corr.), is presented on a flattened cortical reconstruction of one of the subjects. The analysis was carried out within areas that were responsive to either vision or auditory inputs, before or after learning SSA. The statistical parametric map revealed a preference for the pre-learning condition within the right visual cortex, and a preference for the post-learning condition within the left auditory cortex. Retinotopic and tonotopic borders are presented as well; blue lines delineate tonotopic areas and red lines delineate retinotopic areas. (B) Beta values sampled from the clusters depicted in (A) reveal that the learning effect stemmed from changes in crossmodal attenuations (grey dots represent single subjects' beta values; means and SD are presented). In primary visual areas (on the left), visual responses were significantly positive throughout the experiments (*P < 0.05, **P < 0.005, ***P < 0.0005, corr.). However, auditory responses were significantly negative during the Post-passive experiment, underlying the learning effect in this area. In the primary auditory cluster, auditory stimuli elicited significant positive responses throughout the experiments, but visual responses were negative in the “Pre” and “Plus” experiments. (C) Auditory responses in the visual cortex (blue box, left) and visual responses in the auditory cortex (red box, right) in all 3 experimental conditions (Pre, Post, and Plus, in left to right panels), compared with baseline. In all cases, only negative responses were detected, if any (P < 0.05, uncorrected). Here, as well tonotopic borders are in blue and retinotopic borders are depicted in red. In the visual cortex, auditory responses were not presented before learning SSA, but appeared both after learning and in the audiovisual integration task. This experimental context-dependent crossmodal effect underlies the preference of the visual cortex for the pre-learning condition. In the auditory cortex, a mirror pattern appeared with visual attenuation before learning and not afterwards. This release of attenuation explains the preference in the auditory cortex for the post-learning. In the Plus experiment, both crossmodal effects were apparent.
Mentions: We used the ANOVA learning effect to chart the changes in sensory responses following learning (Table 1, learning effect). Post hoc analysis was carried out to examine the direction of the effect, and post-learning conditions (auditory and visual) were compared with the pre-learning conditions (Fig. 3A). The learning effect was examined within areas which were positively responsive to either auditory or visual stimuli. A significant preference for post-learning conditions was found in the right PT (Brodmann 41), and a significant preference for the pre-learning conditions was found in the left Inferior Occipital Gyrus (IOG, Brodmann 19; Fig. 3A, P < 0.05, corr.). The positive cluster in the auditory cortex was located well within the areas responsive to auditory stimuli as defined by the ANOVA modality effect (Fig. 2A, in blue), and was on the border of the tonotopic responsive areas with some of it within and some outside. This indicates that the learning effect was not only in the primary auditory area, but also in the associative auditory areas (Striem-Amit et al. 2011), in line with previous crossmodal effect reports in the auditory cortex (Foxe et al. 2002; Kayser et al. 2008). The visual cluster lay within the retinotopic boundaries in the foveal part of area V3 and LO. To better understand these learning effects, the GLM-evaluated beta values were sampled from these areas (Fig. 3B). Auditory and visual beta values from the 3 experimental conditions (“Pre,” “Post,” and “Plus”) were tested for significant responses, and the results were corrected for multiple comparisons using a false discovery rate (FDR) correction. In the left IOG, positive beta values were found for visual conditions in all 3 experiments. However, the auditory responses were not significantly different from zero before learning and were significantly negative in the “Post” condition. This suggests that the preference for the pre-learning condition found in visual areas was due to the auditory attenuations (as suggested by the negative beta values) in this area after learning the visual-to-auditory SSA. It should be noted that negative beta values do not necessarily mean a negative BOLD signal, but rather attenuations of the positive signal. In this case, visual responses in visual areas were significantly lower, yet still positive, when accompanied by auditory stimuli after SSA learning, compared with times when those were not accompanied by auditory stimuli (see Methods for further details).Figure 3.

Bottom Line: Secondly, associative areas changed their sensory response profile from strongest response for visual to that for auditory.Consistent features were also found in the sensory dominance in sensory areas and audiovisual convergence in associative area Middle Temporal Gyrus.These 2 factors allow for both stability and a fast, dynamic tuning of the system when required.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical Neurobiology, Institute for Medical Research Israel-Canada (IMRIC), Hadassah Medical School, Hebrew University of Jerusalem, Jerusalem 91220, Israel Interdisciplinary Center for Neural Computation, The Edmond & Lily Safra Center for Brain Sciences (ELSC), Hebrew University of Jerusalem, Jerusalem 91905, Israel.

No MeSH data available.


Related in: MedlinePlus