Linking hippocampal CA3 sequences and spatial representations

• Applicant: Professor Dr. Christian Leibold
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2019 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 419289665

• Final Report Year: 2024

Final Report Abstract

The mammalian hippocampus hosts temporally ordered neural activations that can be decoded as spatial trajectories. The function of such activity “sequences” is still largely enigmatic. Theories connect hippocampal sequences with planning, navigation and also memory consolidation. There is, however, also evidence of sequence activity that can be decoded as spatial trajectories in environments never seen so far, which let us assume that sensory-motor experience, at the time of occurrence, is mapped to preexisting sequences. In this completed research project, we developed computational models showing that this latter idea is plausible and at the same time made predictions we could verify in experimental data. Our modelling and analysis, e.g., showed that some sequences are predominantly visible if an animal moves in a certain direction and that these direction dependent temporal correlations predominantly establish themselves in hippocampal area CA3. Moreover, we could show that preexisting sequences are useful for learning spatial representations that suffice for navigation tasks and that such intrinsic sequencs can serve as detectable movement direction-independent landmark signals despite the presence of dominant sensory motor driven place cell activity. Thus, small modulations of hippocampal place cell activity contain reliable spatial information concurrently to encoding movement in space.

Publications

• A Model for Navigation in Unknown Environments Based on a Reservoir of Hippocampal Sequences.
  Leibold, Christian
  
• A model for navigation in unknown environments based on a reservoir of hippocampal sequences. Neural Networks, 124, 328-342.
  Leibold, Christian
  
• Directional Tuning of Phase Precession Properties in the Hippocampus.
  Yiu, Yuk-Hoi; Leutgeb, Jill K. & Leibold, Christian
  
• Distinct directional modulations of hippocampal theta scale spike timing in areas CA1 and CA3. Cosyne 2021
  Y.-H. Yiu, J.K. Leutgeb & C. Leibold
  
• Graded remapping of hippocampal ensembles under sensory conflicts. Cell Reports, 36(11), 109661.
  Fetterhoff, Dustin; Sobolev, Andrey & Leibold, Christian
  
• Directional Tuning of Phase Precession Properties in the Hippocampus. The Journal of Neuroscience, 42(11), 2282-2297.
  Yiu, Yuk-Hoi; Leutgeb, Jill K. & Leibold, Christian
  
• Neural Kernels for Recursive Support Vector Regression as a Model for Episodic Memory.
  Leibold, Christian
  
• Neural kernels for recursive support vector regression as a model for episodic memory. Biological Cybernetics, 116(3), 377-386.
  Leibold, Christian
  
• Theta Sequences in a 2D Space: An Integrated Model of Extrinsic and Intrinsic Encoding in the Hippocampus. Bernstein Conference 2023; IV 134
  Y.-H. Yiu & C. Leibold
  
• A theory of hippocampal theta correlations accounting for extrinsic and intrinsic sequences. eLife, 12.
  Yiu, Yuk-Hoi & Leibold, Christian
  
• A Theory of Hippocampal Theta Correlations: Extrinsic and Intrinsic Sequences.
  Yiu, Yuk-Hoi & Leibold, Christian
  
• Encoding 2D space with extrinsic and intrinsic theta sequences: A hippocampus model. SFN 2023; PSTR438.14 / VV48
  Y.-H. Yiu & C. Leibold
  
• Rigid theta sequences in the hippocampal CA3 area shape phase precession directionality in 2-D space. 7th HBP Student Conference, Madrid
  Y.-H. Yiu, J. Leutgeb & C. Leibold