Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations

• Published in: Nature communications Vol. 11; no. 1; p. 2217
• Main Authors: Navas-Olive, Andrea, Valero, Manuel, Jurado-Parras, Teresa, de Salas-Quiroga, Adan, Averkin, Robert G., Gambino, Giuditta, Cid, Elena, de la Prida, Liset M.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 05.05.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 13/51; 631/114/116/2392; 631/378/3920; 64/110; 64/60; 64/86; 9/30; 9/97; Action Potentials - physiology; Algorithms; Animals; Behavior; CA1 Region, Hippocampal - cytology; CA1 Region, Hippocampal - physiology; Cell morphology; Computational neuroscience; Computer Simulation; Constraining; Cytology; Evolutionary algorithms; Female; Frequency dependence; Genetic algorithms; Glutamatergic transmission; Hippocampus; Humanities and Social Sciences; Identification methods; Kinetics; Locking; Male; Memory; Memory tasks; Mental task performance; Mice, Inbred C57BL; Mice, Transgenic; Models, Neurological; Morphology; multidisciplinary; Neurons - physiology; Oscillations; Patch-Clamp Techniques; Population; Pyramidal cells; Pyramidal Cells - physiology; Rats, Wistar; Representations; Science; Science (multidisciplinary); Selectivity; Synapses - physiology; Theta Rhythm - physiology; Theta rhythms; Variance analysis
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-15840-6

Theta oscillations play a major role in temporarily defining the hippocampal rate code by translating behavioral sequences into neuronal representations. However, mechanisms constraining phase timing and cell-type-specific phase preference are unknown. Here, we employ computational models tuned with evolutionary algorithms to evaluate phase preference of individual CA1 pyramidal cells recorded in mice and rats not engaged in any particular memory task. We applied unbiased and hypothesis-free approaches to identify effects of intrinsic and synaptic factors, as well as cell morphology, in determining phase preference. We found that perisomatic inhibition delivered by complementary populations of basket cells interacts with input pathways to shape phase-locked specificity of deep and superficial pyramidal cells. Somatodendritic integration of fluctuating glutamatergic inputs defined cycle-by-cycle by unsupervised methods demonstrated that firing selection is tuneable across sublayers. Our data identify different mechanisms of phase-locking selectivity that are instrumental for flexible dynamical representations of theta sequences. Theta oscillations have been implicated in hippocampal processing but mechanisms constraining phase timing of specific cell types are unknown. Here, the authors combine single-cell and multisite recordings with evolutionary computational models to evaluate mechanisms of phase preference of deep and superficial CA1 pyramidal cells.