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A functional topography within the cholinergic basal forebrain for processing sensory cues associated with reward and punishment

View ORCID ProfileBlaise Robert, Eyal Y. Kimchi, Yurika Watanabe, Tatenda Chakoma, Miao Jing, Yulong Li, View ORCID ProfileDaniel B. Polley
doi: https://doi.org/10.1101/2021.04.16.439895
Blaise Robert
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston MA 02114 USA
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  • ORCID record for Blaise Robert
Eyal Y. Kimchi
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston MA 02114 USA
2Dept. Neurology, Massachusetts General Hospital, Boston MA 02114
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Yurika Watanabe
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston MA 02114 USA
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Tatenda Chakoma
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston MA 02114 USA
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Miao Jing
3Chinese Institute for Brain Research, Beijing 102206, China
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Yulong Li
4State Key Laboratory of Membrane Biology, Peking University School of Life Sciences; PKU-IDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences, Beijing 100871, China
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Daniel B. Polley
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston MA 02114 USA
5Dept. Otolaryngology - Head and Neck Surgery, Harvard Medical School, Boston MA 02114 USA
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  • ORCID record for Daniel B. Polley
  • For correspondence: daniel_polley@meei.harvard.edu
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Abstract

Basal forebrain cholinergic neurons (BFCNs) project throughout the cortex to regulate arousal, stimulus salience, plasticity, and learning. The basal forebrain features distinct connectivity along its anteroposterior axis that could impart regional differences in feature processing. Here, we simultaneously measured bulk BFCN activity from an anterior structure, the horizontal limb of the diagonal band (HDB), and from the posterior tail of the basal forebrain in globus pallidus and substantia innominata (GP/SI) over a 30-day period as mice learned a sensory reversal task. Although HDB and GP/SI responses were similar for many features, HDB more closely tracked fluctuations in pupil-indexed brain state and exhibited stronger responses to reward omission than to delivery of anticipated awards. In GP/SI, BFCNs were strongly activated by sound, and this response was further enhanced for punishment-predicting – but not reward-predicting – cues. These results identify a functional topography that diversifies cholinergic modulatory signals broadcast to downstream brain regions.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted April 19, 2021.
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A functional topography within the cholinergic basal forebrain for processing sensory cues associated with reward and punishment
Blaise Robert, Eyal Y. Kimchi, Yurika Watanabe, Tatenda Chakoma, Miao Jing, Yulong Li, Daniel B. Polley
bioRxiv 2021.04.16.439895; doi: https://doi.org/10.1101/2021.04.16.439895
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A functional topography within the cholinergic basal forebrain for processing sensory cues associated with reward and punishment
Blaise Robert, Eyal Y. Kimchi, Yurika Watanabe, Tatenda Chakoma, Miao Jing, Yulong Li, Daniel B. Polley
bioRxiv 2021.04.16.439895; doi: https://doi.org/10.1101/2021.04.16.439895

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