Dichotomous activity and function of neurons with low- and high-frequency discharge in the external globus pallidus of non-human primates

Shiran Katabi; Avital Adler; Marc Deffains; Hagai Bergman

doi:10.1016/j.celrep.2022.111898

Dichotomous activity and function of neurons with low- and high-frequency discharge in the external globus pallidus of non-human primates

Shiran Katabi^*, Avital Adler, Marc Deffains, Hagai Bergman

^*Corresponding author for this work

Edmond & Lily Safra Center for Brain Sciences

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

3 Scopus citations

Abstract

To date, there is a consensus that there are at least two neuronal populations in the non-human primate (NHP) external globus pallidus (GPe): low-frequency discharge (LFD) and high-frequency discharge (HFD) neurons. Nevertheless, almost all NHP physiological studies have neglected the functional importance of LFD neurons. This study examined the discharge features of these two GPe neuronal subpopulations recorded in four NHPs engaged in a classical conditioning task with cues predicting reward, neutral and aversive outcomes. The results show that LFD neurons tended to burst, encoded the salience of behavioral cues, and exhibited correlated spiking activity. By contrast, the HFD neurons tended to pause, encoded cue valence, and exhibited uncorrelated spiking activity. Overall, these findings point to the dichotomic organization of the NHP GPe, which is likely to be critical to the implementation of normal basal ganglia functions and computations.

Original language	American English
Article number	111898
Journal	Cell Reports
Volume	42
Issue number	1
DOIs	https://doi.org/10.1016/j.celrep.2022.111898
State	Published - 31 Jan 2023

Bibliographical note

Funding Information:
We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research (CNRS) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation, the TRR295 Rune German Science Centers Project, the Rosetrees Foundation, and the Simone and Bernard Guttman Chair in Brain Research (to H.B.). S.K. and H.B. designed the research. S.K. A.A. and M.D. collected the data. S.K. analyzed and interpreted the data. S.K. M.D. and H.B. wrote the manuscript. All authors read and commented on the final version of the manuscript. The authors declare no competing interests.

Funding Information:
We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research ( CNRS ) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation , the TRR295 Rune German Science Centers Project, the Rosetrees Foundation , and the Simone and Bernard Guttman Chair in Brain Research (to H.B.).

Publisher Copyright:
© 2022 The Authors

Keywords

CP: Neuroscience
basal ganglia
behavior
dichotomous organization
electrophysiology
globus pallidus
information processing
non-human primates
single-unit recordings

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10.1016/j.celrep.2022.111898

Cite this

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title = "Dichotomous activity and function of neurons with low- and high-frequency discharge in the external globus pallidus of non-human primates",

abstract = "To date, there is a consensus that there are at least two neuronal populations in the non-human primate (NHP) external globus pallidus (GPe): low-frequency discharge (LFD) and high-frequency discharge (HFD) neurons. Nevertheless, almost all NHP physiological studies have neglected the functional importance of LFD neurons. This study examined the discharge features of these two GPe neuronal subpopulations recorded in four NHPs engaged in a classical conditioning task with cues predicting reward, neutral and aversive outcomes. The results show that LFD neurons tended to burst, encoded the salience of behavioral cues, and exhibited correlated spiking activity. By contrast, the HFD neurons tended to pause, encoded cue valence, and exhibited uncorrelated spiking activity. Overall, these findings point to the dichotomic organization of the NHP GPe, which is likely to be critical to the implementation of normal basal ganglia functions and computations.",

keywords = "CP: Neuroscience, basal ganglia, behavior, dichotomous organization, electrophysiology, globus pallidus, information processing, non-human primates, single-unit recordings",

author = "Shiran Katabi and Avital Adler and Marc Deffains and Hagai Bergman",

note = "Funding Information: We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research (CNRS) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation, the TRR295 Rune German Science Centers Project, the Rosetrees Foundation, and the Simone and Bernard Guttman Chair in Brain Research (to H.B.). S.K. and H.B. designed the research. S.K. A.A. and M.D. collected the data. S.K. analyzed and interpreted the data. S.K. M.D. and H.B. wrote the manuscript. All authors read and commented on the final version of the manuscript. The authors declare no competing interests. Funding Information: We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research ( CNRS ) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation , the TRR295 Rune German Science Centers Project, the Rosetrees Foundation , and the Simone and Bernard Guttman Chair in Brain Research (to H.B.). Publisher Copyright: {\textcopyright} 2022 The Authors",

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T1 - Dichotomous activity and function of neurons with low- and high-frequency discharge in the external globus pallidus of non-human primates

AU - Katabi, Shiran

AU - Adler, Avital

AU - Deffains, Marc

AU - Bergman, Hagai

N1 - Funding Information: We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research (CNRS) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation, the TRR295 Rune German Science Centers Project, the Rosetrees Foundation, and the Simone and Bernard Guttman Chair in Brain Research (to H.B.). S.K. and H.B. designed the research. S.K. A.A. and M.D. collected the data. S.K. analyzed and interpreted the data. S.K. M.D. and H.B. wrote the manuscript. All authors read and commented on the final version of the manuscript. The authors declare no competing interests. Funding Information: We thank Dr. Yaron Dagan and Dr. Tamar Ravins for assistance with animal care, Dr. Atira Bick for assistance with the coordination and execution of the MRI, and Esther Singer for editing. We also thank Anatoly Shapochnikov for help in preparing the experimental setup and Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. This work was supported by the Nehemia Levtzion Fellowship and the Foulkes Foundation (to S.K.); the French National Research Agency (ANR) and the French National Center for Scientific Research ( CNRS ) (to M.D.); the Israel Science Foundation (ISF), the Israel-China BiNational Scientific Foundation , the TRR295 Rune German Science Centers Project, the Rosetrees Foundation , and the Simone and Bernard Guttman Chair in Brain Research (to H.B.). Publisher Copyright: © 2022 The Authors

PY - 2023/1/31

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N2 - To date, there is a consensus that there are at least two neuronal populations in the non-human primate (NHP) external globus pallidus (GPe): low-frequency discharge (LFD) and high-frequency discharge (HFD) neurons. Nevertheless, almost all NHP physiological studies have neglected the functional importance of LFD neurons. This study examined the discharge features of these two GPe neuronal subpopulations recorded in four NHPs engaged in a classical conditioning task with cues predicting reward, neutral and aversive outcomes. The results show that LFD neurons tended to burst, encoded the salience of behavioral cues, and exhibited correlated spiking activity. By contrast, the HFD neurons tended to pause, encoded cue valence, and exhibited uncorrelated spiking activity. Overall, these findings point to the dichotomic organization of the NHP GPe, which is likely to be critical to the implementation of normal basal ganglia functions and computations.

AB - To date, there is a consensus that there are at least two neuronal populations in the non-human primate (NHP) external globus pallidus (GPe): low-frequency discharge (LFD) and high-frequency discharge (HFD) neurons. Nevertheless, almost all NHP physiological studies have neglected the functional importance of LFD neurons. This study examined the discharge features of these two GPe neuronal subpopulations recorded in four NHPs engaged in a classical conditioning task with cues predicting reward, neutral and aversive outcomes. The results show that LFD neurons tended to burst, encoded the salience of behavioral cues, and exhibited correlated spiking activity. By contrast, the HFD neurons tended to pause, encoded cue valence, and exhibited uncorrelated spiking activity. Overall, these findings point to the dichotomic organization of the NHP GPe, which is likely to be critical to the implementation of normal basal ganglia functions and computations.

KW - CP: Neuroscience

KW - basal ganglia

KW - behavior

KW - dichotomous organization

KW - electrophysiology

KW - globus pallidus

KW - information processing

KW - non-human primates

KW - single-unit recordings

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DO - 10.1016/j.celrep.2022.111898

M3 - Article

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JO - Cell Reports

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ER -

Dichotomous activity and function of neurons with low- and high-frequency discharge in the external globus pallidus of non-human primates

Abstract

Bibliographical note

Keywords

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