RESUBMISSION: Neural processing underlying auditory pattern recognition in an insect brain

重新提交：昆虫大脑中听觉模式识别的神经处理

• 批准号: BB/J01835X/1
• 负责人: Berthold Hedwig
• 金额: $ 39.39万
• 依托单位: University of Cambridge
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2013
• 资助国家: 英国
• 起止时间: 2013 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FJ01835X%2F1
• 关键词: RESUBMISSION; Neural; processing; underlying; auditory

Neuroscience aims at understanding how sensory pathways are organised, how stimuli are processed and how features are extracted to elicit an appropriate motor response. Especially in intraspecific communication the recognition of specific stimulus features plays an important role as species-specific olfactory, visual and/or acoustic signals are employed for mate attraction and rivalry behaviour. As sounds are always transient, signalling by repetitive patterns of pulses is central to acoustic communication in many vertebrates and invertebrates. Especially frogs and insects like bush-crickets and crickets use simple sound pulses generated with species-specific temporal patterns for communication. In the auditory pathway of the receiver, these signals require neural filter mechanisms that respond to the temporal structure of sound patterns. Considerable progress has been made in frogs in describing brain neurons with selective tuning to pulse patterns. However, there is still a very limited understanding of neurons underlying temporal processing of sound patterns in crickets although since decades they are a model system for insect hearing. Female crickets are attracted to the species-specific pattern of male calling song. In behavioural experiments we demonstrated the tuning of their phonotactic behaviour to changes in pulse interval, pulse duration and chirp interval. For example their phonotactic behaviour is tuned to the pulse pattern of the male song as pulses with shorter or longer periods are not attractive. We now aim to understand at the level of identified neurons the filter mechanisms in the brain that allow the recognition of the species-specific song pattern.The ascending auditory interneuron that forwards the pulse pattern of the calling song from the first thoracic ganglion to the brain exhibits no filter properties. Hypothesis for temporal filtering in the brain have been put forward, however, the actual neural mechanisms have not been revealed. In preliminary experiments we identified local brain neurons which form a ring-like auditory neuropil in the protocerebrum matching the axonal arborisations of the ascending interneuron. Some of these neurons showed a selective response to the pulse interval of the calling song and received inhibitory and excitatory synaptic inputs. In other systems the interaction between inhibition and excitation is crucial for selectivity to pulse patterns. Using the same acoustic paradigms as in the behavioural studies we will analyse the activity of auditory brain neurons. We will focus on four questions: 1). Which brain neurons are involved in temporal filtering of acoustic pulse patterns?2). What are the neural mechanisms underlying temporal filtering? 3). What is the structural and functional organisation of the auditory neuropil?4). Which projection neurons connect the auditory neuropil to other brain regions?The project will be based on our experience of recording intracellularly the activity of auditory brain neurons with sharp microelectrodes. The neural responses will be compared with our behavioural data and quantitative analysis will reveal to what degree the activity of single neurons mirrors the behavioural tuning. The pattern of inhibitory and excitatory synaptic activity will provide crucial information on how temporal filtering is achieved within the auditory network. We will manipulate the membrane potential of neurons by intracellular current injection to analyse the nature of the neural filter mechanisms in detail. Finally we will use confocal microscopy to reveal the structural details of these neurons in the brain and we will identify neurons which link the auditory neuropil to other areas of the brain. The analysis of the pattern recognition network in crickets will provide insight to principle mechanisms of temporal filtering at the level of identified neurons and can be a model for temporal selectivity in other systems.

神经科学旨在了解感觉通路是如何组织的，刺激是如何处理的，以及如何提取特征以引起适当的运动反应。特别是在种内交流中，对特定刺激特征的识别起着重要的作用，因为物种特有的嗅觉、视觉和/或声音信号被用来吸引配偶和竞争行为。由于声音总是短暂的，通过重复的脉冲模式发出信号是许多脊椎动物和无脊椎动物声音交流的核心。尤其是青蛙和像灌木蟋蟀和蟋蟀这样的昆虫，它们利用物种特有的时间模式产生的简单声音脉冲进行交流。在接受者的听觉通路中，这些信号需要神经过滤机制来响应声音模式的时间结构。在描述具有选择性调整脉冲模式的大脑神经元方面，青蛙已经取得了相当大的进展。然而，尽管几十年来它们是昆虫听觉的模型系统，但对蟋蟀声音模式的时间处理背后的神经元的理解仍然非常有限。雌性蟋蟀被雄性蟋蟀特有的鸣叫模式所吸引。在行为实验中，我们证明了它们的声致性行为随着脉冲间隔、脉冲持续时间和啁啾间隔的变化而变化。例如，它们的音致性行为是根据雄性歌曲的脉冲模式来调整的，因为周期较短或较长的脉冲都没有吸引力。我们现在的目标是在已识别的神经元水平上了解大脑中允许识别物种特定鸣声模式的过滤机制。从第一胸神经节向大脑传递鸣叫声脉冲模式的上升听觉中间神经元没有过滤特性。人们提出了大脑时间过滤的假说，但其实际的神经机制尚未揭示。在初步实验中，我们发现在原大脑中形成环状听神经的局部脑神经元与上行中间神经元的轴突树突相匹配。其中一些神经元对鸣叫声的脉冲间隔表现出选择性反应，并接受抑制性和兴奋性突触输入。在其他系统中，抑制和激发之间的相互作用对脉冲模式的选择性至关重要。使用与行为研究相同的声学范式，我们将分析听觉脑神经元的活动。我们将重点关注四个问题：1)。哪些脑神经元参与声脉冲模式的时间过滤？时间过滤背后的神经机制是什么？3）. 听神经的结构和功能组织是什么？哪些投射神经元连接听神经和大脑其他区域？这个项目将基于我们用尖锐的微电极记录大脑听觉神经元细胞内活动的经验。神经反应将与我们的行为数据进行比较，定量分析将揭示单个神经元的活动在多大程度上反映了行为调节。抑制性和兴奋性突触活动的模式将提供听觉网络中时间过滤是如何实现的关键信息。我们将通过细胞内电流注入来操纵神经元的膜电位，以详细分析神经过滤机制的性质。最后，我们将使用共聚焦显微镜来揭示大脑中这些神经元的结构细节，我们将识别连接听神经和大脑其他区域的神经元。对蟋蟀模式识别网络的分析将提供在已识别神经元水平上对时间过滤的原理机制的见解，并可以作为其他系统中时间选择性的模型。

项目成果

Song pattern recognition in crickets based on a delay-line and coincidence-detector mechanism.

• DOI: 10.1098/rspb.2017.0745
• 发表时间: 2017-05-31
• 期刊: Proceedings. Biological sciences
• 作者: Hedwig B;Sarmiento-Ponce EJ
• 通讯作者: Sarmiento-Ponce EJ

A small, computationally flexible network produces the phenotypic diversity of song recognition in crickets.

• DOI: 10.7554/elife.61475
• 发表时间: 2021-11-11
• 期刊: eLife
• 影响因子: 7.7
• 作者: Clemens J;Schöneich S;Kostarakos K;Hennig RM;Hedwig B
• 通讯作者: Hedwig B

Auditory pattern recognition and steering in the cricket Teleogryllus oceanicus

蟋蟀 Teleogryllus oceanicus 的听觉模式识别和转向

• DOI: 10.1111/phen.12043
• 发表时间: 2014
• 期刊: Physiological Entomology
• 影响因子: 1.5
• 作者: CROS E