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Spatial representation by ramping activity of neurons in the retrohippocampal cortex

Sarah A. Tennant, Harry Clark, Ian Hawes, Wing Kin Tam, Junji Hua, Wannan Yang, Klara Z. Gerlei, Emma R. Wood, Matthew F. Nolan
doi: https://doi.org/10.1101/2021.03.15.435518
Sarah A. Tennant
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
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  • For correspondence: stennan2@exseed.ed.ac.uk mattnolan@ed.ac.uk
Harry Clark
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Ian Hawes
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Wing Kin Tam
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, United Kingdom
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Junji Hua
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Wannan Yang
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
4Center for Neural Science, New York University, New York, United States
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Klara Z. Gerlei
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Emma R. Wood
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, United Kingdom
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Matthew F. Nolan
1Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, United Kingdom
3Centre for Statistics, University of Edinburgh, Edinburgh, United Kingdom
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  • For correspondence: stennan2@exseed.ed.ac.uk mattnolan@ed.ac.uk
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Summary

Neurons in the retrohippocampal cortices play crucial roles in spatial memory. Many retrohippocampal neurons have firing fields that are selectively active at specific locations, with memory for rewarded locations associated with reorganisation of these firing fields. Whether this is the sole strategy for representing spatial memories is unclear. Here, we demonstrate that during a spatial memory task retrohippocampal neurons encode location through ramping activity that extends within segments of a linear track approaching and following a reward, with the rewarded location represented by offsets or switches in the slope of the ramping activity. These ramping representations could be maintained independently of trial outcome and cues that mark the reward location, indicating that they result from recall of the track structure. During recordings in an open arena, neurons that generated ramping activity during the spatial memory task were more numerous than grid or border cells, with a majority showing spatial firing that did not meet criteria for classification as grid or border representations. Encoding of rewarded locations through offsets and switches in the slope of ramping activity also emerged in recurrent neural networks trained to solve a similar location memory task. Impaired performance of these networks following disruption of outputs from ramping neurons is consistent with this coding strategy supporting navigation to recalled locations of behavioural significance. We hypothesise that retrohippocampal ramping activity mediates readout of learned models for goal-directed navigation.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵6 Lead contact

  • Modified methods for generating shuffled control data (Figure 1) and for model fitting (Figure 2). Additional simulation experiments to examine consequences of perturbation of the model network (Figure 7). Numerous minor changes.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 26, 2022.
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Spatial representation by ramping activity of neurons in the retrohippocampal cortex
Sarah A. Tennant, Harry Clark, Ian Hawes, Wing Kin Tam, Junji Hua, Wannan Yang, Klara Z. Gerlei, Emma R. Wood, Matthew F. Nolan
bioRxiv 2021.03.15.435518; doi: https://doi.org/10.1101/2021.03.15.435518
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Spatial representation by ramping activity of neurons in the retrohippocampal cortex
Sarah A. Tennant, Harry Clark, Ian Hawes, Wing Kin Tam, Junji Hua, Wannan Yang, Klara Z. Gerlei, Emma R. Wood, Matthew F. Nolan
bioRxiv 2021.03.15.435518; doi: https://doi.org/10.1101/2021.03.15.435518

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