Control and recalibration of path integration in place cells using optic flow

Manu S Madhav; Ravikrishnan P Jayakumar; Brian Y Li; Shahin G Lashkari; Kelly Wright; Francesco Savelli; James J Knierim; Noah J Cowan

doi:10.1038/s41593-024-01681-9

Control and recalibration of path integration in place cells using optic flow

Nat Neurosci. 2024 Aug;27(8):1599-1608. doi: 10.1038/s41593-024-01681-9. Epub 2024 Jun 27.

Authors

Manu S Madhav^#^{1

2

3

4

5}, Ravikrishnan P Jayakumar^#^{6

7

8}, Brian Y Li⁶, Shahin G Lashkari^{7

8}, Kelly Wright⁶, Francesco Savelli^{6

9}, James J Knierim^{10

11

12}, Noah J Cowan^{13

14}

Affiliations

¹ Mind/Brain Institute, Johns Hopkins University, Baltimore, MD, USA. [email protected].
² Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USA. [email protected].
³ Laboratory for Computational Sensing and Robotics, Johns Hopkins University, Baltimore, MD, USA. [email protected].
⁴ School of Biomedical Engineering, University of British Columbia, Vancouver, British Columbia, Canada. [email protected].
⁵ Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada. [email protected].
⁶ Mind/Brain Institute, Johns Hopkins University, Baltimore, MD, USA.
⁷ Laboratory for Computational Sensing and Robotics, Johns Hopkins University, Baltimore, MD, USA.
⁸ Mechanical Engineering Department, Johns Hopkins University, Baltimore, MD, USA.
⁹ Department of Neuroscience, Developmental and Regenerative Biology, The University of Texas at San Antonio, San Antonio, TX, USA.
¹⁰ Mind/Brain Institute, Johns Hopkins University, Baltimore, MD, USA. [email protected].
¹¹ Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USA. [email protected].
¹² Solomon H. Snyder Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA. [email protected].
¹³ Laboratory for Computational Sensing and Robotics, Johns Hopkins University, Baltimore, MD, USA. [email protected].
¹⁴ Mechanical Engineering Department, Johns Hopkins University, Baltimore, MD, USA. [email protected].

^# Contributed equally.

Abstract

Hippocampal place cells are influenced by both self-motion (idiothetic) signals and external sensory landmarks as an animal navigates its environment. To continuously update a position signal on an internal 'cognitive map', the hippocampal system integrates self-motion signals over time, a process that relies on a finely calibrated path integration gain that relates movement in physical space to movement on the cognitive map. It is unclear whether idiothetic cues alone, such as optic flow, exert sufficient influence on the cognitive map to enable recalibration of path integration, or if polarizing position information provided by landmarks is essential for this recalibration. Here, we demonstrate both recalibration of path integration gain and systematic control of place fields by pure optic flow information in freely moving rats. These findings demonstrate that the brain continuously rebalances the influence of conflicting idiothetic cues to fine-tune the neural dynamics of path integration, and that this recalibration process does not require a top-down, unambiguous position signal from landmarks.

MeSH terms

Animals
Cues
Hippocampus / cytology
Hippocampus / physiology
Male
Optic Flow* / physiology
Place Cells* / physiology
Rats
Rats, Long-Evans*
Space Perception / physiology

Abstract

MeSH terms

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