Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation
Eric Lowet,
Daniel J. Sheehan,
Ulises Chialva,
Rodrigo De Oliveira Pena,
Rebecca A. Mount,
Sheng Xiao,
Samuel L. Zhou,
Hua-an Tseng,
Howard Gritton,
Sanaya Shroff,
Krishnakanth Kondabolu,
Cyrus Cheung,
Yangyang Wang,
Kiryl D. Piatkevich,
Edward S. Boyden,
Jerome Mertz,
Michael E. Hasselmo,
Horacio G. Rotstein,
Xue Han
Affiliations
Eric Lowet
Department of Biomedical Engineering, Boston University, Boston, MA, USA; Corresponding author
Daniel J. Sheehan
Department of Psychological and Brain Sciences, Boston University, Boston, MA, USA
Ulises Chialva
Departamento de Matemática, Universidad Nacional del Sur, Buenos Aires, Argentina
Rodrigo De Oliveira Pena
Federated Department of Biological Sciences, New Jersey Institute of Technology & Rutgers University, Newark, NJ, USA
Rebecca A. Mount
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Sheng Xiao
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Samuel L. Zhou
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Hua-an Tseng
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Howard Gritton
Department of Comparative Biosciences, University of Illinois at Urbana–Champaign, Urbana, IL, USA
Sanaya Shroff
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Krishnakanth Kondabolu
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Cyrus Cheung
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Yangyang Wang
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Kiryl D. Piatkevich
School of Life Sciences, Westlake University, Westlake Laboratory of Life Sciences and Biomedicine, Westlake Institute for Advanced Study, Hangzhou, Zhejiang, China
Edward S. Boyden
McGovern Institute for Brain Research and Howard Hughes Medical Institute, MIT, Cambridge, MA, USA
Jerome Mertz
Department of Biomedical Engineering, Boston University, Boston, MA, USA
Michael E. Hasselmo
Department of Psychological and Brain Sciences, Boston University, Boston, MA, USA
Horacio G. Rotstein
Federated Department of Biological Sciences, New Jersey Institute of Technology & Rutgers University, Newark, NJ, USA
Xue Han
Department of Biomedical Engineering, Boston University, Boston, MA, USA; Corresponding author
Summary: Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3–12 Hz) and encode an animal’s position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30–100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.
