Stimulus competition and visuospatial selection: Neural circuit and computational mechanisms

刺激竞争和视觉空间选择：神经回路和计算机制

• 批准号: 10701900
• 负责人: Shreesh P Mysore
• 金额: $ 45.76万
• 依托单位: JOHNS HOPKINS UNIVERSITY
• 依托单位国家: 美国
• 财政年份: 2017
• 资助国家: 美国
• 起止时间: 2017-03-01 至 2026-05-31
• 项目状态: 未结题
• 来源: https://reporter.nih.gov/project-details/10701900
• 关键词: Address; Anatomy; Animals; Area; Attention; Attention deficit hyperactivity disorder; Barn Owls; Behavior; Birds; Brain; Categories; Cell Nucleus; Cells; Code; Complement; Complex; Computer Models; Data; Decision Making; Distant; Electrophysiology (science); Environment; Feedback; Functional disorder; Glutamates; Head; Homologous Gene; Injections; Iontophoresis; Logic; Mammals; Maps; Mental disorders; Methods; Midbrain structure; Monkeys; Muscarinics; Neurons; Neurotransmitters; Noise; Pattern; Perception; Process; Protocols documentation; Regulation; Resistance; Role; Route; Runaway; Schizophrenia; Sensory; Signal Transduction; Site; Source; Stains; Stimulus; Synapses; System; Tectum Mesencephali; Testing; Tracer; Visuospatial; Work; analytical tool; anatomical tracing; autism spectrum disorder; awake; cholinergic; cholinergic neuron; cholinergic synapse; design; experimental study; extracellular; in vivo; inhibitory neuron; insight; neural; neural circuit; neuromechanism; neuroregulation; neurotransmission; novel; predictive modeling; prevent; receptive field; response; sensory stimulus; simulation; superior colliculus Corpora quadrigemina; visual stimulus

PROJECT SUMMARY Animals routinely operate in complex environments rich in sensory stimuli. They handle this informational complexity by having their behavior guided by the most salient (and more generally, highest priority) stimulus in the environment. The neural circuit mechanisms underlying competitive selection of the highest priority stimulus across space remain poorly understood. Recent evidence from behaving monkeys has revealed that the intermediate and deep layers of the superior colliculus (SCid), a major sensorimotor hub in the vertebrate midbrain, are required for normal competitive stimulus selection. In parallel, our work in the barn owl optic tectum (OTid, avian homolog of SCid) has revealed that OTid neurons signal the highest priority stimulus categorically, which can account for SCid’s critical role in spatial selection behavior. Such categorical signaling requires a specialized, donut-like pattern of spatial inhibition onto OTid from an inhibitory nucleus called Imc in the nearby midbrain isthmic complex. Separately, feedback from a cholinergic isthmic nucleus, Ipc, is known to amplify OTid firing rates. Despite these insights, several fundamental questions about the functional logic of this isthmo-tectal (OT-Imc-Ipc) network for competitive stimulus selection remain open, and here, we address three. First, we aim to elucidate how the preferential neural signaling of the most salient stimulus is implemented in OTid. Specifically, our hypotheses are (1a) that OTid signals the strongest among competing stimuli with a combination of enhanced gamma synchrony, reduced trial-trial variability, greater resistance to adaptation, and reduced noise correlations (rather than just with elevated firing rates), and (1b) that cholinergic Ipc serves as a multiplexed mechanism for regulating these diverse OTid coding features. Second, we aim to elucidate a neuromodulatory mechanism for the control of categorization. Our hypotheses (based on our model predictions) are (2a) that (hitherto uncharacterized) spatially-specific cholinergic input onto Imc neurons causes multiplicative modulation of Imc activity, and (2b) that it serves as a mechanism to enhance the degree of categorical signaling of the most salient stimulus by OTid. Third, we aim to uncover the source and broader functional logic of this cholinergic input. Our hypotheses are (3a) that Ipc is the dominant source of cholinergic input onto Imc neurons, and (3b) that in parallel, Ipc, which influences activity across the layers of the OT, selectively spares the OT layer that provides input to it (layer 10); revealing a precisely organized circuit design that minimizes runaway feedback excitation in this network. We will test these hypotheses using in vivo electrophysiology and drug iontophoresis during visual stimulus presentation in awake, head-fixed barn owls, together with computational modeling. Preliminary data from the three aims support our hypotheses. Results from the proposed work have the power to reveal fundamental neural circuit mechanisms involving multiple neurotransmitter systems for executing the sophisticated computations that underlie stimulus competition and spatial selection across space.

项目摘要 动物通常在富含感觉刺激的复杂环境中起作用。他们处理这个信息 复杂性通过其行为受到最显着（并且更普遍，最高优先级）刺激的指导 环境。最高优先级刺激的竞争选择的神经回路机制 跨太空仍然很少了解。猴子的最新证据表明 上丘（SCID）的中间和深层，脊椎动物中的主要感觉运动集线器 中脑是正常竞争刺激选择所必需的。同时，我们在谷仓猫头鹰光学底部的工作 （OTID，SCID的鸟类同源物）已经揭示了OTID神经元明确地表明了优先型刺激， 这可以解释SCID在空间选择行为中的关键作用。这样的分类信号需要 从附近的抑制性核对OTID上的专业，甜甜圈样模式 中脑静脉复合体。另外，已知来自胆碱能静脉核IPC的反馈可以扩增otid 发射率。尽管有这些见解，但有关此地峡直肠功能逻辑的几个基本问​​题 （OT-IMC-IPC）竞争性刺激选择网络保持开放，在这里，我们解决了三个。首先，我们的目标 为了阐明在OTID中如何实现最突出的刺激的首选中性信号。具体来说， 我们的假设是（1a），OTID信号在竞争刺激中强烈，结合了增强 伽马同步，降低试验可变性，更大的适应性和降低的噪声相关性 （而不是仅以升高率升高）和（1B）胆碱能IPC充当多重机制 调节这些潜水员OTID编码功能。第二，我们旨在阐明一种神经调节机制 类别的控制。我们的假设（基于我们的模型预测）是（2a）（迄今为止 在IMC神经元上的空间特异性胆碱能输入引起IMC的乘法调节 活动，（2b）它是增强最突出的分类信号程度的机制 OTID刺激。第三，我们旨在发现该胆碱能输入的源和更广泛的功能逻辑。我们的 假设是（3A）IPC是IMC神经元中胆碱能输入的主要来源，而（3B） 并行，影响OT层跨层的活动的IPC，有选择地避免提供的OT层 输入它（第10层）;揭示精确组织的电路设计，可最大程度地减少失控的反馈兴奋 在这个网络中。我们将使用体内电生理学和药物离子疗法测试这些假设 醒着，头部固定谷仓猫头鹰的视觉刺激表现，以及计算建模。初步的 来自三个目标的数据支持我们的假设。拟议工作的结果有能力揭示 与多个神经递质系统有关的基本神经递质系统用于执行 刺激竞争和跨空间空间选择的复杂计算。

项目成果

Distinct neural mechanisms construct classical versus extraclassical inhibitory surrounds in an inhibitory nucleus in the midbrain attention network.

• DOI: 10.1038/s41467-023-39073-5
• 发表时间: 2023-06-09
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Schryver, Hannah M.;Mysore, Shreesh P.
• 通讯作者: Mysore, Shreesh P.

Donut-like organization of inhibition underlies categorical neural responses in the midbrain.

• DOI: 10.1038/s41467-022-29318-0
• 发表时间: 2022-03-30
• 期刊: Nature communications
• 影响因子: 16.6
• 作者: Mahajan NR;Mysore SP
• 通讯作者: Mysore SP

Categorical Signaling of the Strongest Stimulus by an Inhibitory Midbrain Nucleus.

抑制性中脑核最强刺激的分类信号传导。

• DOI: 10.1523/jneurosci.0042-20.2020
• 发表时间: 2020
• 期刊: The Journal of neuroscience : the official journal of the Society for Neuroscience
• 作者: Schryver,HannahM;Straka,Malgorzata;Mysore,ShreeshP
• 通讯作者: Mysore,ShreeshP

Spatial Dependence of Stimulus Competition in the Avian Nucleus Isthmi Pars Magnocellularis.

禽类细胞核 Isthmi Pars Magnocellularis 刺激竞争的空间依赖性。

• DOI: 10.1159/000500192
• 发表时间: 2019
• 期刊: Brain, behavior and evolution
• 作者: Schryver,HannahM;Mysore,ShreeshP
• 通讯作者: Mysore,ShreeshP