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Reliable and efficient processing of sensory information at body temperature by rodent cortical neurons

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Abstract

Some pathological conditions, such as infections and febrile seizures, may cause temperature fluctuations in the brain. We ask here how these temperature fluctuations, particularly hypothermia and hyperthermia, affect the cortical information coding performance and response reliability of warm-blooded animals. We studied this issue by a combination of in vitro whole-cell patch clamp recordings from cortical pyramidal neurons and computational simulations of Hodgkin–Huxley cortical neuronal model at different temperatures. A significantly higher reliability of the neuronal response to repeated input signals was observed at physiological temperature (\(\sim 35\,^{\circ }\hbox {C}\)) than that at a much lower temperature (\(\sim 24\,^{\circ }\hbox {C}\)) or upon hyperthermia (\(\sim 41\,^{\circ }\hbox {C}\)). In addition, the firing rate of excitatory neurons (i.e., pyramidal neurons) was increased gradually, while it decreased gradually for inhibitory neurons (e.g., PV interneurons) as the temperature increased from 25 to \(40\,^{\circ }\hbox {C}\). The opposite changes in the response activity level between pyramidal neurons and interneurons suggested a shift in the excitatory/inhibitory (E/I) balance in the local network circuit as a function of changing temperature. An analysis of the information coding efficiency suggested that the pyramidal neurons displayed the maximal response reliability with the highest coding efficiency and information transmission rate at body temperature, suggesting that the E/I balance observed at this temperature might be optimal for enhancing information coding in cortical neurons. In addition, we applied tetrodotoxin and 4-aminopyridine to partially block \(\hbox {Na}^{+}\) and \(\hbox {K}^{+}\) channels, respectively, and observed that a change in sodium or potassium conductance could also alter the neuronal response reliability of pyramidal neurons.

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Acknowledgements

YY thanks for the support from the National Natural Science Foundation of China (81761128011, 31571070), the Shanghai Municipal Science and Technology Major Project (No. 2018SHZDZX01) and ZJLab, the Shanghai Science and Technology Committee support (16410722600), and the program for the Professor of Special Appointment (Eastern Scholar SHH1140004) at Shanghai Institutions of Higher Learning.

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Authors and Affiliations

  1. College of Biosciences, Fudan University, Shanghai, 200433, China

    Xin Fu

  2. State Key Laboratory of Medical Neurobiology, School of Life Science and Human Phenome Institute, Institutes of Brain Science, Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, 200433, China

    Yuguo Yu

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  1. Xin Fu
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YY supervised the research, YY and XF designed the research, XF and YY performed the experimental study and data analysis, and XF and YY wrote the paper. All authors reviewed the manuscript.

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Correspondence to Yuguo Yu.

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The conducts and procedures involving animal experiments in this study were approved by the Animal Ethics Committee of Fudan University School of Life Sciences.

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Fu, X., Yu, Y. Reliable and efficient processing of sensory information at body temperature by rodent cortical neurons. Nonlinear Dyn 98, 215–231 (2019). https://doi.org/10.1007/s11071-019-05184-2

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