Similarity in Neuronal Firing Regimes across Mammalian Species
- Yasuhiro Mochizuki1,
- Tomokatsu Onaga1,
- Hideaki Shimazaki2,
- Takeaki Shimokawa3,
- Yasuhiro Tsubo2,4,
- Rie Kimura5,
- Akiko Saiki5,
- Yutaka Sakai5,
- Yoshikazu Isomura5,
- Shigeyoshi Fujisawa2,
- Ken-ichi Shibata6,
- Daichi Hirai6,
- Takahiro Furuta6,
- Takeshi Kaneko6,
- Susumu Takahashi8,
- Tomoaki Nakazono8,
- Seiya Ishino9,
- Yoshio Sakurai8,
- Takashi Kitsukawa11,
- Jong Won Lee12,
- Hyunjung Lee13,
- Min Whan Jung12,14,
- Cecilia Babul15,
- Pedro E. Maldonado15,
- Kazutaka Takahashi16,
- Fritzie I. Arce-McShane16,
- Callum F. Ross16,
- Barry J. Sessle18,
- Nicholas G. Hatsopoulos16,17,
- Thomas Brochier19,
- Alexa Riehle19,20,
- Paul Chorley20,
- Sonja Grün20,21,
- Hisao Nishijo22,
- Satoe Ichihara-Takeda23,
- Shintaro Funahashi7,
- Keisetsu Shima24,
- Hajime Mushiake24,
- Yukako Yamane11,25,
- Hiroshi Tamura11,25,
- Ichiro Fujita11,25,
- Naoko Inaba6,
- Kenji Kawano6,
- Sergei Kurkin26,
- Kikuro Fukushima26,
- Kiyoshi Kurata27,
- Masato Taira28,
- Ken-Ichiro Tsutsui29,
- Tadashi Ogawa10,
- Hidehiko Komatsu10,
- Kowa Koida30,
- Keisuke Toyama3,
- Barry J. Richmond31, and
- Shigeru Shinomoto1
- 1Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan,
- 2RIKEN Brain Science Institute, Saitama 351-0198, Japan,
- 3ATR Neural Information Analysis Laboratories, Kyoto 619-0288, Japan,
- 4Department of Human and Computer Intelligence, Ritsumeikan University, Shiga 525-8577, Japan,
- 5Brain Science Institute, Tamagawa University, Tokyo 194-8610, Japan,
- 6Graduate School of Medicine and
- 7Kokoro Research Center, Kyoto University, Kyoto 606-8501, Japan,
- 8Graduate School of Brain Science, Doshisha University, Kyoto 610-0394, Japan,
- 9Department of Developmental Physiology and
- 10Division of Sensory and Cognitive Information, National Institute for Physiological Sciences, Aichi 444-8585, Japan,
- 11Graduate School of Frontier Biosciences, Osaka University, Osaka 565-0871, Japan,
- 12Center for Synaptic Brain Dysfunctions, Institute for Basic Science, Daejeon 305-701, Korea,
- 13Kyungpook National University School of Medicine, Daegu 700-422, Korea,
- 14Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Korea,
- 15Biomedical Neuroscience Institute, Universidad de Chile, Santiago 8380453, Chile,
- 16Department of Organismal Biology and Anatomy and
- 17Committee of Computational Neuroscience, University of Chicago, Chicago, Illinois 60637,
- 18Faculty of Dentistry, University of Toronto, Toronto M5G 1G6, Canada,
- 19Institut de Neurosciences de la Timone, CNRS-AMU, Marseille 13005, France,
- 20Institute of Neuroscience and Medicine (INM-6) & Institute for Advanced Simulation (IAS-6) & JARA Brain Institute I, Jülich 52425, Germany,
- 21Theoretical Systems Neurobiology, RWTH Aachen University, Aachen 52056, Germany,
- 22Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama 930-0194, Japan,
- 23School of Health Science, Sapporo Medical University, Sapporo 060-8556, Japan,
- 24Department of Physiology, School of Medicine, Tohoku University, Sendai 980-8575, Japan,
- 25Center for Information and Neural Networks, Osaka University and National Institute of Information and Communications Technology, Osaka 565-0871, Japan,
- 26Department of Physiology, School of Medicine, Hokkaido University, Sapporo 060-8638, Japan,
- 27Department of Physiology, Hirosaki University Graduate School of Medicine, Hirosaki 036-8562, Japan,
- 28Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo 113-8549, Japan,
- 29Laboratory of Systems Neuroscience, Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, Japan,
- 30Electronics-Inspired Interdisciplinary Research Institute, Toyohashi University of Technology, Aichi 441-8580, Japan, and
- 31Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892
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Author contributions: Y.M., B.J.R., and S.S. designed research; Y.T., R.K., A.S., Y. Sakai, Y.I., S. Fujisawa, K.-i.S., D.H., T.F., T. Kaneko, S.T., T.N., S.I., Y. Sakurai, T. Kitsukawa, J.W.L., H.L., M.W.J., C.B., P.E.M., K. Takahashi, F.I.A.-M., C.F.R., B.J.S., N.G.H., T.B., A.R., P.C., S.G., H.N., S.I.-T., S. Funahashi, K.S., H.M., Y.Y., H.T., I.F., N.I., K. Kawano, S.K., K.F., K. Kurata, M.T., K.-I.T., T. Ogawa, H.K., K. Koida, and K. Toyama performed research; Y.M., T. Onaga, H.S., and T.S. analyzed data; B.J.R. and S.S. wrote the paper.
Abstract
The architectonic subdivisions of the brain are believed to be functional modules, each processing parts of global functions. Previously, we showed that neurons in different regions operate in different firing regimes in monkeys. It is possible that firing regimes reflect differences in underlying information processing, and consequently the firing regimes in homologous regions across animal species might be similar. We analyzed neuronal spike trains recorded from behaving mice, rats, cats, and monkeys. The firing regularity differed systematically, with differences across regions in one species being greater than the differences in similar areas across species. Neuronal firing was consistently most regular in motor areas, nearly random in visual and prefrontal/medial prefrontal cortical areas, and bursting in the hippocampus in all animals examined. This suggests that firing regularity (or irregularity) plays a key role in neural computation in each functional subdivision, depending on the types of information being carried.
SIGNIFICANCE STATEMENT By analyzing neuronal spike trains recorded from mice, rats, cats, and monkeys, we found that different brain regions have intrinsically different firing regimes that are more similar in homologous areas across species than across areas in one species. Because different regions in the brain are specialized for different functions, the present finding suggests that the different activity regimes of neurons are important for supporting different functions, so that appropriate neuronal codes can be used for different modalities.
- firing irregularity/regularity
- interspecies similarity
- neuronal firing pattern
- neuronal firing regime
- Received January 22, 2016.
- Revision received April 10, 2016.
- Accepted April 12, 2016.
- Copyright © 2016 the authors 0270-6474/16/365737-12$15.00/0
