Supramammillary neurons projecting to the septum regulate dopamine and motivation for environmental interaction in mice

Andrew J. Kesner, Rick Shin, Coleman B. Calva, Reuben F. Don, Sue Junn, Christian T. Potter, Leslie A. Ramsey, Ahmed F. Abou-Elnaga, Christopher G. Cover, Dong V. Wang, Hanbing Lu, Yihong Yang and Satoshi Ikemoto ()
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Andrew J. Kesner: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Rick Shin: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Coleman B. Calva: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Reuben F. Don: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Sue Junn: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Christian T. Potter: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Leslie A. Ramsey: Ex Vivo Electrophysiology Core, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Ahmed F. Abou-Elnaga: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Christopher G. Cover: Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Dong V. Wang: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Hanbing Lu: Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Yihong Yang: Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health
Satoshi Ikemoto: Behavioral Neuroscience Research Branch, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health

Nature Communications, 2021, vol. 12, issue 1, 1-18

Abstract: Abstract The supramammillary region (SuM) is a posterior hypothalamic structure, known to regulate hippocampal theta oscillations and arousal. However, recent studies reported that the stimulation of SuM neurons with neuroactive chemicals, including substances of abuse, is reinforcing. We conducted experiments to elucidate how SuM neurons mediate such effects. Using optogenetics, we found that the excitation of SuM glutamatergic (GLU) neurons was reinforcing in mice; this effect was relayed by their projections to septal GLU neurons. SuM neurons were active during exploration and approach behavior and diminished activity during sucrose consumption. Consistently, inhibition of SuM neurons disrupted approach responses, but not sucrose consumption. Such functions are similar to those of mesolimbic dopamine neurons. Indeed, the stimulation of SuM-to-septum GLU neurons and septum-to-ventral tegmental area (VTA) GLU neurons activated mesolimbic dopamine neurons. We propose that the supramammillo-septo-VTA pathway regulates arousal that reinforces and energizes behavioral interaction with the environment.

Date: 2021
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DOI: 10.1038/s41467-021-23040-z

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