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Spike-timing pattern operates as gamma-distribution across cell types, regions and animal species and is essential for naturally-occurring cognitive states

Meng Li, Kun Xie, Hui Kuang, Jun Liu, Deheng Wang, Grace E. Fox, Wei Wei, Xiaojian Li, Yuhui Li, Fang Zhao, Liang Chen, Zhifeng Shi, He Cui, Ying Mao, Joe Z. Tsien
doi: https://doi.org/10.1101/145813
Meng Li
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Kun Xie
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Hui Kuang
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Jun Liu
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Deheng Wang
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Grace E. Fox
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Wei Wei
3The Brain Decoding Center, BanNa Biomedical Research Institute, Yunnan Academy of Science and Technology, Yunnan 666106, China
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Xiaojian Li
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Yuhui Li
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Fang Zhao
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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Liang Chen
4Neuropathology, Huashan Hospital, Fudan University, Shanghai 200040, China
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Zhifeng Shi
4Neuropathology, Huashan Hospital, Fudan University, Shanghai 200040, China
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He Cui
2Institute of Neuroscience, Chinese Academy of Sciences, Shanghai 200031, China
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Ying Mao
4Neuropathology, Huashan Hospital, Fudan University, Shanghai 200040, China
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Joe Z. Tsien
3The Brain Decoding Center, BanNa Biomedical Research Institute, Yunnan Academy of Science and Technology, Yunnan 666106, China
1Brain and Behavior Discovery Institute and Department of Neurology, Augusta University, Augusta, GA 30912, USA
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  • For correspondence: jtsien@augusta.edu
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Abstract

Spike-timing patterns - crucial for synaptic plasticity and neural computation - are often modeled as Poisson-like random processes, log-normal distribution or gamma-distribution patterns, each with different underlying assumptions that may or may not be biologically true. However, it is not entirely clear whether (and how well) these different models would or would not capture spike-timing statistical patterns across different neurons, regions, animal species and cognitive states. Here, we examine statistical patterns of spike-timing irregularity in 13 different cortical and subcortical regions from mouse, hamster, cat and monkey brains. In contrast to the widely-assumed Poisson or log-normal distribution patterns, we show that spike-timing patterns of various projection neurons-including cortical excitatory principal cells, hippocampal pyramidal cells, inhibitory striatal medium spiny neurons and dopaminergic neurons, as well as fast-spiking interneurons – all invariantly conform to the gamma-distribution model. While higher regularity in spike-timing patterns are observed in a few cases, such as mouse DA neurons and monkey motor cortical neurons, there is no clear tendency in increased firing regularity from the sensory and subcortical neurons to prefrontal or motor cortices, as previously entertained. Moreover, gamma shapes of spike-timing patterns remain robust over various natural cognitive states, such as sleep, awake periods, or during fearful episodic experiences. Interestingly, ketamine-induced general anesthesia or unconsciousness is associated with the breakdown of forebrain spike patterns from a singular gamma distribution into two distinct subtypes of gamma distributions, suggesting the importance of this spike-timing pattern in supporting natural cognitive states. These results suggest that gamma-distribution patterns of spike timing reflect not only a fundamental property conserved across different neurons, regions and animal species, but also an operation crucial for supporting natural cognitive states. Such gamma-distribution-based spike-timing patterns can also have important implications for real-time neural coding and realistic neuromorphic computing.

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Posted February 09, 2018.
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Spike-timing pattern operates as gamma-distribution across cell types, regions and animal species and is essential for naturally-occurring cognitive states
Meng Li, Kun Xie, Hui Kuang, Jun Liu, Deheng Wang, Grace E. Fox, Wei Wei, Xiaojian Li, Yuhui Li, Fang Zhao, Liang Chen, Zhifeng Shi, He Cui, Ying Mao, Joe Z. Tsien
bioRxiv 145813; doi: https://doi.org/10.1101/145813
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Spike-timing pattern operates as gamma-distribution across cell types, regions and animal species and is essential for naturally-occurring cognitive states
Meng Li, Kun Xie, Hui Kuang, Jun Liu, Deheng Wang, Grace E. Fox, Wei Wei, Xiaojian Li, Yuhui Li, Fang Zhao, Liang Chen, Zhifeng Shi, He Cui, Ying Mao, Joe Z. Tsien
bioRxiv 145813; doi: https://doi.org/10.1101/145813

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