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Auditory competition and stimulus selection across spatial locations from midbrain to forebrain in barn owls.
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2024-10-29 , DOI: 10.1523/jneurosci.1298-24.2024
Andrea J Bae,Brian J Fischer,José L Peña

Barn owls enable investigation of neural mechanisms underlying stimulus selection of concurrent stimuli. The audio-visual space map in the optic tectum (OT), avian homologue of the superior colliculus, encodes relative strength of concurrent auditory stimuli through spike response rate and interneuronal spike train synchrony (STS). Open questions remain regarding stimulus selection in downstream forebrain regions lacking topographic coding of auditory space, including the functional consequences of interneuronal STS on interregional signaling. To this end, we presented concurrent stimuli at different locations and manipulated relative strength while simultaneously recording neural responses from OT and its downstream thalamic target, nucleus rotundus (nRt), in awake barn owls of both sexes. Results demonstrated that broadly spatially tuned nRt units exhibit different spike response patterns to competition depending on spatial tuning preferences. Modeling suggests nRt units integrate convergent inputs from distant locations across midbrain map regions. Additionally, STS within nRt reflects the temporal properties of the strongest stimulus. Furthermore, interregional STS between OT and nRt was strongest when spatial tuning overlap between units across regions was large and when the strongest stimulus location during competition was favorable for units in both regions. Additionally, though gamma oscillations synthesized within OT are weakly propagated within nRt, average gamma power across regions correlates with strength of interregional STS. Overall, we demonstrate that nRt integrates inputs across distant areas of OT, retains spatial information through differences in strength of inputs from various locations of the midbrain map across neurons, and prioritizes coding of identity features to the strongest sound.Significance Statement The brain strategically selects and preferentially processes salient stimuli. A critical function to this process involves transferring salient information across regions that may exhibit drastic transformations in coding schemes. Our study in barn owls investigates bottom-up signaling between the midbrain space map and its downstream thalamic target, which lacks spatial topography as also observed in mammalian auditory forebrain regions to elucidate general mechanisms underlying how spatial location information and other properties of the strongest sound are relayed between regions. Results show that the thalamus integrates neural responses widely across the midbrain map, retains coding of spatial location through varying strength of inputs of the map across neurons, and prioritizes further coding of identity features only to the strongest sound.

中文翻译:


仓鸮从中脑到前脑的空间位置的听觉竞争和刺激选择。



仓鸮能够研究同时刺激的刺激选择背后的神经机制。视壳 (OT) 中的视听空间图是上丘的鸟类同源物,通过尖峰反应率和神经元间尖峰序列同步 (STS) 编码并发听觉刺激的相对强度。关于缺乏听觉空间地形编码的下游前脑区域的刺激选择仍然存在悬而未决的问题,包括神经元间 STS 对区域间信号的功能影响。为此,我们在不同位置呈现并发刺激并操纵相对强度,同时记录来自两性清醒谷仓猫头鹰的 OT 及其下游丘脑靶点圆形核 (nRt) 的神经反应。结果表明,根据空间调谐偏好,广谱空间调谐的 nRt 单元对竞争表现出不同的尖峰响应模式。建模表明 nRt 单元整合了来自中脑地图区域远处的收敛输入。此外,nRt 中的 STS 反映了最强刺激的时间特性。此外,当跨区域单元之间的空间调谐重叠较大且竞争期间最强的刺激位置对两个区域的单元有利时,OT 和 nRt 之间的区域间 STS 最强。此外,尽管在 OT 中合成的 γ 振荡在 nRt 中传播较弱,但跨区域的平均 gamma 功率与区域间 STS 的强度相关。 总体而言,我们证明 nRt 整合了 OT 遥远区域的输入,通过跨神经元中脑图不同位置的输入强度差异来保留空间信息,并优先将身份特征编码为最强的声音。意义陈述 大脑战略性地选择并优先处理显着的刺激。此过程的一个关键功能涉及跨区域传输显著信息,这些区域可能会在编码方案中表现出剧烈的转变。我们对仓鸮的研究调查了中脑空间图与其下游丘脑目标之间的自下而上的信号传导,该目标缺乏空间地形,正如在哺乳动物听觉前脑区域所观察到的那样,以阐明空间位置信息和最强声音的其他特性如何在区域之间传递的一般机制。结果表明,丘脑在整个中脑图中广泛整合了神经反应,通过跨神经元的图输入的不同强度保留了空间位置的编码,并将身份特征的进一步编码优先于最强的声音。
更新日期:2024-10-29
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