Hoglen Nerissa E G, Larimer Phillip, Phillips Elizabeth A K, Malone Brian J, Hasenstaub Andrea R
Center for Integrative Neuroscience, University of California , San Francisco, California.
Department of Otolaryngology-Head and Neck Surgery, University of California , San Francisco, California.
J Neurophysiol. 2018 May 1;119(5):1753-1766. doi: 10.1152/jn.00101.2017. Epub 2018 Jan 24.
Both mice and primates are used to model the human auditory system. The primate order possesses unique cortical specializations that govern auditory processing. Given the power of molecular and genetic tools available in the mouse model, it is essential to understand the similarities and differences in auditory cortical processing between mice and primates. To address this issue, we directly compared temporal encoding properties of neurons in the auditory cortex of awake mice and awake squirrel monkeys (SQMs). Stimuli were drawn from a sinusoidal amplitude modulation (SAM) paradigm, which has been used previously both to characterize temporal precision and to model the envelopes of natural sounds. Neural responses were analyzed with linear template-based decoders. In both species, spike timing information supported better modulation frequency discrimination than rate information, and multiunit responses generally supported more accurate discrimination than single-unit responses from the same site. However, cortical responses in SQMs supported better discrimination overall, reflecting superior temporal precision and greater rate modulation relative to the spontaneous baseline and suggesting that spiking activity in mouse cortex was less strictly regimented by incoming acoustic information. The quantitative differences we observed between SQM and mouse cortex support the idea that SQMs offer advantages for modeling precise responses to fast envelope dynamics relevant to human auditory processing. Nevertheless, our results indicate that cortical temporal processing is qualitatively similar in mice and SQMs and thus recommend the mouse model for mechanistic questions, such as development and circuit function, where its substantial methodological advantages can be exploited. NEW & NOTEWORTHY To understand the advantages of different model organisms, it is necessary to directly compare sensory responses across species. Contrasting temporal processing in auditory cortex of awake squirrel monkeys and mice, with parametrically matched amplitude-modulated tone stimuli, reveals a similar role of timing information in stimulus encoding. However, disparities in response precision and strength suggest that anatomical and biophysical differences between squirrel monkeys and mice produce quantitative but not qualitative differences in processing strategy.
小鼠和灵长类动物都被用于构建人类听觉系统模型。灵长目动物具有独特的皮质特化结构，可调控听觉处理过程。鉴于小鼠模型中可用的分子和遗传工具的强大功能，了解小鼠和灵长类动物听觉皮质处理过程中的异同至关重要。为解决这一问题，我们直接比较了清醒小鼠和清醒松鼠猴（SQMs）听觉皮质中神经元的时间编码特性。刺激信号取自正弦幅度调制（SAM）范式，该范式此前已被用于表征时间精度和模拟自然声音的包络。使用基于线性模板的解码器分析神经反应。在这两个物种中，与速率信息相比，尖峰时间信息在调制频率辨别方面表现更佳，并且多单元反应通常比来自同一部位的单单元反应支持更准确的辨别。然而，总体而言，SQMs的皮质反应支持更好的辨别，这反映出相对于自发基线而言，其具有更高的时间精度和更大的速率调制，表明小鼠皮质中的尖峰活动受传入声学信息的约束没那么严格。我们在SQMs和小鼠皮质之间观察到的定量差异支持了这样一种观点，即SQMs在模拟与人类听觉处理相关的快速包络动态的精确反应方面具有优势。尽管如此，我们的结果表明，小鼠和SQMs的皮质时间处理在性质上是相似的，因此对于诸如发育和回路功能等机制性问题，推荐使用小鼠模型，因为在这些问题上可以利用其显著的方法学优势。新发现与值得注意之处为了解不同模式生物的优势，有必要直接比较不同物种的感觉反应。通过对清醒松鼠猴和小鼠的听觉皮质进行时间处理对比，并采用参数匹配的调幅音调刺激，揭示了时间信息在刺激编码中具有相似作用。然而，反应精度和强度的差异表明，松鼠猴和小鼠之间的解剖学和生物物理学差异在处理策略上产生了定量而非定性的差异。
