Dynamics of space coding by mouse hippocampal CA1 field neurons in a free navigation task in different environments

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Abstract

The development of persistent cognitive adaptations in neurons is a key area of focus in contemporary neuroscience. A significant illustration of such adaptations occurs through spatial specializations in place cells with one or more receptive fields that are sensitive to spatial cues (place fields) [1].

In prior research, we extensively examined the dynamics of place field formation in granular layer neurons of the CA1 field in the hippocampus of mice during arbitrary free navigation in a circular track [2]. As the primary factor for maintaining stability in the spatial specialization of place cells, we have introduced dynamic selectivity. This approach enables us to monitor the latency of each place field’s formation and the selectivity dynamics of place cells to their respective fields throughout one or multiple shooting sessions. However, in one-dimensional settings, like the circular track referenced previously, place fields can demonstrate direction-specificity with regards to animal movement [3]. This factor considerably complicates the analysis for arbitrary movement trajectories of animals. In this study, additional experiments were conducted to capture the neural activity of mice in two-dimensional environments. The experiments were conducted in both a rectangular field with objects and a circular arena with a varying number of obstacles.

In this paper, we conduct a comparative analysis to examine the critical parameters governing the development of spatial specializations in a one-dimensional circle track and two-dimensional arenas. These parameters include specialization latency, average dynamic selectivity, initial increase in selectivity, and the proportion of “immediate” place fields that remain stable from the first animal visit. The study discovered that the mean selectivity of the place fields escalated in each session, with higher rates observed in subsequent sessions versus the initial session in a novel setting. Additionally, there was a significant occurrence of “immediate” place fields, representing 11% of all place fields in the rounded arena with obstacles, and 25% of all place fields in the circular track.

Additionally, a population analysis of neural activity was performed on the first session in a circular track and a round arena with obstacles. Using Laplace eigenmaps for the dimension reduction of population vectors, the trajectory of animals was reconstructed, and the accuracy of this reconstruction agreed with the average dynamic selectivity for each animal included in the analysis. Thus, dynamic selectivity was verified as a measure of the spatial coding quality of the entire registered population of neurons.

Full Text

The development of persistent cognitive adaptations in neurons is a key area of focus in contemporary neuroscience. A significant illustration of such adaptations occurs through spatial specializations in place cells with one or more receptive fields that are sensitive to spatial cues (place fields) [1].

In prior research, we extensively examined the dynamics of place field formation in granular layer neurons of the CA1 field in the hippocampus of mice during arbitrary free navigation in a circular track [2]. As the primary factor for maintaining stability in the spatial specialization of place cells, we have introduced dynamic selectivity. This approach enables us to monitor the latency of each place field’s formation and the selectivity dynamics of place cells to their respective fields throughout one or multiple shooting sessions. However, in one-dimensional settings, like the circular track referenced previously, place fields can demonstrate direction-specificity with regards to animal movement [3]. This factor considerably complicates the analysis for arbitrary movement trajectories of animals. In this study, additional experiments were conducted to capture the neural activity of mice in two-dimensional environments. The experiments were conducted in both a rectangular field with objects and a circular arena with a varying number of obstacles.

In this paper, we conduct a comparative analysis to examine the critical parameters governing the development of spatial specializations in a one-dimensional circle track and two-dimensional arenas. These parameters include specialization latency, average dynamic selectivity, initial increase in selectivity, and the proportion of “immediate” place fields that remain stable from the first animal visit. The study discovered that the mean selectivity of the place fields escalated in each session, with higher rates observed in subsequent sessions versus the initial session in a novel setting. Additionally, there was a significant occurrence of “immediate” place fields, representing 11% of all place fields in the rounded arena with obstacles, and 25% of all place fields in the circular track.

Additionally, a population analysis of neural activity was performed on the first session in a circular track and a round arena with obstacles. Using Laplace eigenmaps for the dimension reduction of population vectors, the trajectory of animals was reconstructed, and the accuracy of this reconstruction agreed with the average dynamic selectivity for each animal included in the analysis. Thus, dynamic selectivity was verified as a measure of the spatial coding quality of the entire registered population of neurons.

ADDITIONAL INFORMATION

Authors’ contribution. All authors made a substantial contribution to the conception of the work, acquisition, analysis, interpretation of data for the work, drafting and revising the work, final approval of the version to be published and agree to be accountable for all aspects of the work.

Funding sources. The research was carried out with the financial support of the Non-profit Foundation for the Development of Science and Education “Intellect” and the Interdisciplinary Scientific and Educational School of Lomonosov Moscow State University “Brain, Cognitive Systems, Artificial Intelligence”.

Competing interests. The authors declare that they have no competing interests.

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About the authors

V. P. Sotskov

Institute for Advanced Brain Studies, Lomonosov Moscow State University

Author for correspondence.
Email: vsotskov@list.ru
Russian Federation, Moscow

V. V. Plyusnin

Institute for Advanced Brain Studies, Lomonosov Moscow State University

Email: vsotskov@list.ru
Russian Federation, Moscow

N. V. Dokukin

Institute for Advanced Brain Studies, Lomonosov Moscow State University

Email: vsotskov@list.ru
Russian Federation, Moscow

N. A. Pospelov

Institute for Advanced Brain Studies, Lomonosov Moscow State University

Email: vsotskov@list.ru
Russian Federation, Moscow

K. V. Anokhin

Institute for Advanced Brain Studies, Lomonosov Moscow State University; Research Institute of Normal Physiology named after P.K. Anokhin

Email: vsotskov@list.ru
Russian Federation, Moscow; Moscow

References

  1. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34(1):171–175. doi: 10.1016/0006-8993(71)90358-1
  2. Sotskov VP, Pospelov NA, Plusnin VV, Anokhin KV. Calcium imaging reveals fast tuning dynamics of hippocampal place cells and CA1 population activity during free exploration task in mice. Int J Mol Sci. 2022;23(2):638. doi: 10.3390/ijms23020638
  3. McNaughton BL, Barnes CA, O’Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res. 1983;52(1):41–49. doi: 10.1007/BF00237147

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