Auditory and visual interactions between the superior and inferior colliculi in the ferret

Stitt, Iain; Galindo-Leon, Edgar; Pieper, Florian; Hollensteiner, Karl J.; Engler, Gerhard; Engel, Andreas K.

doi:10.1111/ejn.12847

Cited by 15 publications

(13 citation statements)

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“…While consistent with the possibility that visual updating of the perceived direction of a sound source is based on changes in auditory cortical activity, it is also possible that interactions between visual and auditory inputs in the midbrain may be involved. Reciprocal connections exist between the SC and different regions of the inferior colliculus (IC) (Doubell et al, 2000; Stitt et al, 2015), providing a source of retinotopically organized input into the auditory midbrain. Furthermore, auditory responses in the monkey IC are modulated by changes in gaze direction (Zwiers et al, 2004; Gruters and Groh, 2012), implying a role for the midbrain in coordinating neural representations of auditory and visual space.…”

Section: Discussionmentioning

confidence: 99%

Re-weighting of Sound Localization Cues by Audiovisual Training

Kumpik

Campbell

Schnupp

et al. 2019

Preprint

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest Author contribution statement DK, JS and AK conceived and designed the study; DK and CC carried out the experiments and analyzed the data; DK, JS and AK wrote the manuscript. Abstract Word count: 350Sound localization requires the integration in the brain of auditory spatial cues generated by interactions with the external ears, head and body. Perceptual learning studies have shown that the relative weighting of these cues can change in a contextdependent fashion if their relative reliability is altered. One factor that may influence this process is vision, which tends to dominate localization judgments when both modalities are present and induces a recalibration of auditory space if they become misaligned. It is not known, however, whether vision can alter the weighting of individual auditory localization cues. Using non-individualized head-related transfer functions, we measured changes in subjects' sound localization biases and binaural localization cue weights after ~55 minutes of training on an audiovisual spatial oddball task. Four different configurations of spatial congruence between visual and auditory cues (interaural time differences (ITDs) and frequency-dependent interaural level differences (interaural level spectra, ILS) were used. When visual cues were spatially congruent with both auditory spatial cues, we observed an improvement in sound localization, as shown by a reduction in the variance of subjects' localization biases, which was accompanied by an up-weighting of the more salient ILS cue. However, if the position of either one of the auditory cues was randomized during training, no overall improvement in sound localization occurred. Nevertheless, the spatial gain of whichever cue was matched with vision increased, with different effects observed on the gain for the randomized cue depending on whether ITDs or ILS were matched with vision. As a result, we observed a similar up-weighting in ILS when this cue alone was matched with vision, but no overall change in binaural cue weighting when ITDs corresponded to the visual cues and ILS were randomized. Consistently misaligning both cues with vision produced the ventriloquism aftereffect, i.e., a corresponding shift in auditory localization bias, without affecting the variability of the subjects' sound localization judgments, and no overall change in binaural cue weighting. These data show that visual contextual information can invoke a reweighting of auditory localization cues, although concomitant improvements in sound localization are only likely to accompany training with fully congruent audiovisual information. Contribution to the fieldFor the brain to construct a single unified percept of the world, it is necessary that information from our different senses is combined and integrated. This is often thought to be achieved in a statistically optimal fashion with different se...

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Section: Discussionmentioning

confidence: 99%

Re-weighting of Sound Localization Cues by Audiovisual Training

Kumpik

Campbell

Schnupp

et al. 2019

Preprint

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“…Ferrets have been used extensively in physiological and anatomical studies of multisensory processing (e.g. King & Hutchings, 1987;King et al, 1988;King & Schnupp, 2000;Bizley et al, 2007;Bizley & King, 2008;Stitt et al, 2015), but only to a limited degree so far in behavioural experiments (Isaiah et al, 2014;Hollensteiner et al, 2015), despite the ease with which they can be trained to carry out localization and other sensory tasks. We have previously characterized sound localization behaviour in this species by measuring their head-orienting response following stimulus presentation and the subsequent locomotor response as the animals approach the perceived location of the sound source to receive a water reward (Nodal et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Behavioural benefits of multisensory processing in ferrets

Hammond-Kenny

Bajo

King

et al. 2016

Eur J of Neuroscience

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Enhanced detection and discrimination, along with faster reaction times, are the most typical behavioural manifestations of the brain's capacity to integrate multisensory signals arising from the same object. In this study, we examined whether multisensory behavioural gains are observable across different components of the localization response that are potentially under the command of distinct brain regions. We measured the ability of ferrets to localize unisensory (auditory or visual) and spatiotemporally coincident auditory-visual stimuli of different durations that were presented from one of seven locations spanning the frontal hemifield. During the localization task, we recorded the head movements made following stimulus presentation, as a metric for assessing the initial orienting response of the ferrets, as well as the subsequent choice of which target location to approach to receive a reward. Head-orienting responses to auditory-visual stimuli were more accurate and faster than those made to visual but not auditory targets, suggesting that these movements were guided principally by sound alone. In contrast, approach-to-target localization responses were more accurate and faster to spatially congruent auditory-visual stimuli throughout the frontal hemifield than to either visual or auditory stimuli alone. Race model inequality analysis of head-orienting reaction times and approach-totarget response times indicates that different processes, probability summation and neural integration, respectively, are likely to be responsible for the effects of multisensory stimulation on these two measures of localization behaviour.

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“…In turn, anatomical tracings have shown that the inferior colliculus receives visual input from the SC, as well as from retina and visual cortex [ 69 – 72 ], although a recent study in mouse indicates that retinal projections to the inferior colliculus are sparse [ 39 ]. Furthermore, electrophysiological analyses of the anesthesized ferret suggest that the source of the visual responses in the inferior colliculus is the SC rather than direct input from the retina or cortex [ 73 ]. Therefore, it is unlikely that absence of the inferior colliculus would directly affect RGC numbers and axonal projections to the SC in AP-2δ−/− mice; however, it is highly likely that absence of the inferior colliculus can affect SC response, especially as related to visual and auditory signal integration in midbrain.…”

Section: Discussionmentioning

confidence: 99%

Loss of AP-2delta reduces retinal ganglion cell numbers and axonal projections to the superior colliculus

Gaillard

Monckton

et al. 2016

Mol Brain

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BackgroundAP-2δ is the most divergent member of the Activating Protein-2 (TFAP2) family of transcription factors. AP-2δ is restricted to specific regions of the CNS, including a subset of ganglion cells in the retina. Retinal ganglion cells (RGCs), the only output neurons of the retina, are responsible for transmitting the visual signal to the brain.ResultsAP-2δ knockout results in loss of Brn3c (Pou4f3) expression in AP-2δ -positive RGCs. While AP-2δ-/- mice have morphologically normal retinas at birth, there is a significant reduction in retinal ganglion cell numbers by P21, after eye opening. Chromatin immunoprecipitation indicates that Brn3c is a target of AP-2δ in the retina. Using fluorochrome-conjugated cholera toxin subunit B to trace ganglion cell axons from the eye to the major visual pathways in the brain, we found 87 % and 32 % decreases in ipsilateral and contralateral projections, respectively, to the superior colliculus in AP-2δ-/- mice. In agreement with anatomical data, visually evoked responses recorded from the brain confirmed that retinal outputs to the brain are compromised.ConclusionsAP-2δ is important for the maintenance of ganglion cell numbers in the retina. Loss of AP-2δ alters retinal axonal projections to visual centers of the brain, with ipsilaterial projections to the superior colliculus being the most dramatically affected. Our results have important implications for integration of the visual signal at the superior colliculus.Electronic supplementary materialThe online version of this article (doi:10.1186/s13041-016-0244-0) contains supplementary material, which is available to authorized users.

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Auditory and visual interactions between the superior and inferior colliculi in the ferret

Cited by 15 publications

References 50 publications

Re-weighting of Sound Localization Cues by Audiovisual Training

Re-weighting of Sound Localization Cues by Audiovisual Training

Behavioural benefits of multisensory processing in ferrets

Loss of AP-2delta reduces retinal ganglion cell numbers and axonal projections to the superior colliculus

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