Parvalbumin-expressing basal forebrain neurons mediate learning from negative experience

Panna Hegedüs, Bálint Király, Dániel Schlingloff, Victoria Lyakhova, Anna Velencei, Írisz Szabó, Márton I. Mayer, Zsofia Zelenak, Gábor Nyiri and Balázs Hangya ()
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Panna Hegedüs: HUN-REN Institute of Experimental Medicine
Bálint Király: HUN-REN Institute of Experimental Medicine
Dániel Schlingloff: HUN-REN Institute of Experimental Medicine
Victoria Lyakhova: HUN-REN Institute of Experimental Medicine
Anna Velencei: HUN-REN Institute of Experimental Medicine
Írisz Szabó: HUN-REN Institute of Experimental Medicine
Márton I. Mayer: HUN-REN Institute of Experimental Medicine
Zsofia Zelenak: HUN-REN Institute of Experimental Medicine
Gábor Nyiri: HUN-REN Institute of Experimental Medicine
Balázs Hangya: HUN-REN Institute of Experimental Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract Parvalbumin (PV)-expressing GABAergic neurons of the basal forebrain (BFPVNs) were proposed to serve as a rapid and transient arousal system, yet their exact role in awake behaviors remains unclear. We performed bulk calcium measurements and electrophysiology with optogenetic tagging from the horizontal limb of the diagonal band of Broca (HDB) while male mice were performing an associative learning task. BFPVNs responded with a distinctive, phasic activation to punishment, but showed slower and delayed responses to reward and outcome-predicting stimuli. Optogenetic inhibition during punishment impaired the formation of cue-outcome associations, suggesting a causal role of BFPVNs in associative learning. BFPVNs received strong inputs from the hypothalamus, the septal complex and the median raphe region, while they synapsed on diverse cell types in key limbic structures, where they broadcasted information about aversive stimuli. We propose that the arousing effect of BFPVNs is recruited by aversive stimuli to serve crucial associative learning functions.

Date: 2024
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DOI: 10.1038/s41467-024-48755-7

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