Stellate Cells in the Medial Entorhinal Cortex Are Required for Spatial Learning

Sarah A. Tennant; Lukas Fischer; Derek L.F. Garden; Klára Zsófia Gerlei; Cristina Martinez-Gonzalez; Christina McClure; Emma R. Wood; Matthew F. Nolan

doi:10.1016/j.celrep.2018.01.005

Stellate Cells in the Medial Entorhinal Cortex Are Required for Spatial Learning

Sarah A. Tennant, Lukas Fischer, Derek L.F. Garden, Klára Zsófia Gerlei, Cristina Martinez-Gonzalez, Christina McClure, Emma R. Wood, Matthew F. Nolan^* (Corresponding Author)

^*Corresponding author for this work

Medical Sciences

Research output: Contribution to journal › Article › peer-review

42 Citations (Scopus)

Abstract

Spatial learning requires estimates of location that may be obtained by path integration or from positional cues. Grid and other spatial firing patterns of neurons in the superficial medial entorhinal cortex (MEC) suggest roles in behavioral estimation of location. However, distinguishing the contributions of path integration and cue-based signals to spatial behaviors is challenging, and the roles of identified MEC neurons are unclear. We use virtual reality to dissociate linear path integration from other strategies for behavioral estimation of location. We find that mice learn to path integrate using motor-related self-motion signals, with accuracy that decreases steeply as a function of distance. We show that inactivation of stellate cells in superficial MEC impairs spatial learning in virtual reality and in a real world object location recognition task. Our results quantify contributions of path integration to behavior and corroborate key predictions of models in which stellate cells contribute to location estimation.

Original language	English
Pages (from-to)	1313-1324
Journal	Cell Reports
Volume	22
Issue number	5
Early online date	30 Jan 2018
DOIs	https://doi.org/10.1016/j.celrep.2018.01.005
Publication status	Published - Jan 2018

Bibliographical note

Acknowledgments
We thank Ian Duguid for advice in establishing head fixation and treadmill technologies, Gülşen Sürmeli for assistance in targeting of L2SCs, and Jessica Menzies and Michelle Haglund for collecting the object recognition and object location data. This work was supported by the BBSRC (BB/L010496/1 and a BBSRC Eastbio studentship [grant BB/M010996/1]), the Human Frontiers Science Program (RGP0062/2014), and the Wellcome Trust (200855/Z/16/Z and WT093295MA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability Statement

Supplemental Information includes Supplemental Experimental Procedures,
six figures, and one movie and can be found with this article online at
https://doi.org/10.1016/j.celrep.2018.01.005.

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Cite this

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title = "Stellate Cells in the Medial Entorhinal Cortex Are Required for Spatial Learning",

abstract = "Spatial learning requires estimates of location that may be obtained by path integration or from positional cues. Grid and other spatial firing patterns of neurons in the superficial medial entorhinal cortex (MEC) suggest roles in behavioral estimation of location. However, distinguishing the contributions of path integration and cue-based signals to spatial behaviors is challenging, and the roles of identified MEC neurons are unclear. We use virtual reality to dissociate linear path integration from other strategies for behavioral estimation of location. We find that mice learn to path integrate using motor-related self-motion signals, with accuracy that decreases steeply as a function of distance. We show that inactivation of stellate cells in superficial MEC impairs spatial learning in virtual reality and in a real world object location recognition task. Our results quantify contributions of path integration to behavior and corroborate key predictions of models in which stellate cells contribute to location estimation.",

author = "Tennant, {Sarah A.} and Lukas Fischer and Garden, {Derek L.F.} and Gerlei, {Kl{\'a}ra Zs{\'o}fia} and Cristina Martinez-Gonzalez and Christina McClure and Wood, {Emma R.} and Nolan, {Matthew F.}",

note = "Acknowledgments We thank Ian Duguid for advice in establishing head fixation and treadmill technologies, G{\"u}l{\c s}en S{\"u}rmeli for assistance in targeting of L2SCs, and Jessica Menzies and Michelle Haglund for collecting the object recognition and object location data. This work was supported by the BBSRC (BB/L010496/1 and a BBSRC Eastbio studentship [grant BB/M010996/1]), the Human Frontiers Science Program (RGP0062/2014), and the Wellcome Trust (200855/Z/16/Z and WT093295MA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. ",

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AU - Martinez-Gonzalez, Cristina

AU - McClure, Christina

AU - Wood, Emma R.

AU - Nolan, Matthew F.

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N2 - Spatial learning requires estimates of location that may be obtained by path integration or from positional cues. Grid and other spatial firing patterns of neurons in the superficial medial entorhinal cortex (MEC) suggest roles in behavioral estimation of location. However, distinguishing the contributions of path integration and cue-based signals to spatial behaviors is challenging, and the roles of identified MEC neurons are unclear. We use virtual reality to dissociate linear path integration from other strategies for behavioral estimation of location. We find that mice learn to path integrate using motor-related self-motion signals, with accuracy that decreases steeply as a function of distance. We show that inactivation of stellate cells in superficial MEC impairs spatial learning in virtual reality and in a real world object location recognition task. Our results quantify contributions of path integration to behavior and corroborate key predictions of models in which stellate cells contribute to location estimation.

AB - Spatial learning requires estimates of location that may be obtained by path integration or from positional cues. Grid and other spatial firing patterns of neurons in the superficial medial entorhinal cortex (MEC) suggest roles in behavioral estimation of location. However, distinguishing the contributions of path integration and cue-based signals to spatial behaviors is challenging, and the roles of identified MEC neurons are unclear. We use virtual reality to dissociate linear path integration from other strategies for behavioral estimation of location. We find that mice learn to path integrate using motor-related self-motion signals, with accuracy that decreases steeply as a function of distance. We show that inactivation of stellate cells in superficial MEC impairs spatial learning in virtual reality and in a real world object location recognition task. Our results quantify contributions of path integration to behavior and corroborate key predictions of models in which stellate cells contribute to location estimation.

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ER -

Stellate Cells in the Medial Entorhinal Cortex Are Required for Spatial Learning

Abstract

Bibliographical note

Data Availability Statement

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