Mouse hippocampal CA1 VIP interneurons detect novelty in the environment and support recognition memory

In the CA1 hippocampus, vasoactive intestinal polypeptide-expressing interneurons (VIP-INs) play a prominent role in disinhibitory circuit motifs. However, the specific behavioral conditions that lead to circuit disinhibition remain uncertain. To investigate the behavioral relevance of VIP-IN activi...

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Published inCell reports (Cambridge) Vol. 43; no. 4; p. 114115
Main Authors Tamboli, Suhel, Singh, Sanjay, Topolnik, Dimitry, El Amine Barkat, Mohamed, Radhakrishnan, Risna, Guet-McCreight, Alexandre, Topolnik, Lisa
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.04.2024
Elsevier
Subjects
Animals
CA1 Region, Hippocampal - cytology
CA1 Region, Hippocampal - metabolism
CA1 Region, Hippocampal - physiology
CP: Neuroscience
Exploratory Behavior - physiology
Interneurons - metabolism
Interneurons - physiology
Male
Memory - physiology
Mice
Mice, Inbred C57BL
Parvalbumins - metabolism
Pyramidal Cells - metabolism
Pyramidal Cells - physiology
Recognition, Psychology - physiology
Somatostatin - metabolism
Vasoactive Intestinal Peptide - metabolism
CP: Neuroscience
Online AccessGet full text

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Abstract In the CA1 hippocampus, vasoactive intestinal polypeptide-expressing interneurons (VIP-INs) play a prominent role in disinhibitory circuit motifs. However, the specific behavioral conditions that lead to circuit disinhibition remain uncertain. To investigate the behavioral relevance of VIP-IN activity, we employed wireless technologies allowing us to monitor and manipulate their function in freely behaving mice. Our findings reveal that, during spatial exploration in new environments, VIP-INs in the CA1 hippocampal region become highly active, facilitating the rapid encoding of novel spatial information. Remarkably, both VIP-INs and pyramidal neurons (PNs) exhibit increased activity when encountering novel changes in the environment, including context- and object-related alterations. Concurrently, somatostatin- and parvalbumin-expressing inhibitory populations show an inverse relationship with VIP-IN and PN activity, revealing circuit disinhibition that occurs on a timescale of seconds. Thus, VIP-IN-mediated disinhibition may constitute a crucial element in the rapid encoding of novelty and the acquisition of recognition memory. [Display omitted] •Hippocampal CA1 VIP-INs shape spatial exploration by detecting novelty•VIP-INs and pyramidal neurons (PNs) are co-active when encountering novel changes•VIP-IN and PN co-activity inversely scales with activity of SST-INs and PV-INs•VIP-IN-mediated disinhibition supports novelty encoding and recognition memory Tamboli et al. discover “novelty cells” in the mouse hippocampal CA1 area that belong to a family of vasoactive intestinal polypeptide-expressing interneurons (VIP-INs). In freely behaving mice, VIP-INs become highly active during spatial exploration in novel environments, enabling rapid encoding of spatial information and regulating the recognition memory.
AbstractList In the CA1 hippocampus, vasoactive intestinal polypeptide-expressing interneurons (VIP-INs) play a prominent role in disinhibitory circuit motifs. However, the specific behavioral conditions that lead to circuit disinhibition remain uncertain. To investigate the behavioral relevance of VIP-IN activity, we employed wireless technologies allowing us to monitor and manipulate their function in freely behaving mice. Our findings reveal that, during spatial exploration in new environments, VIP-INs in the CA1 hippocampal region become highly active, facilitating the rapid encoding of novel spatial information. Remarkably, both VIP-INs and pyramidal neurons (PNs) exhibit increased activity when encountering novel changes in the environment, including context- and object-related alterations. Concurrently, somatostatin- and parvalbumin-expressing inhibitory populations show an inverse relationship with VIP-IN and PN activity, revealing circuit disinhibition that occurs on a timescale of seconds. Thus, VIP-IN-mediated disinhibition may constitute a crucial element in the rapid encoding of novelty and the acquisition of recognition memory. [Display omitted] •Hippocampal CA1 VIP-INs shape spatial exploration by detecting novelty•VIP-INs and pyramidal neurons (PNs) are co-active when encountering novel changes•VIP-IN and PN co-activity inversely scales with activity of SST-INs and PV-INs•VIP-IN-mediated disinhibition supports novelty encoding and recognition memory Tamboli et al. discover “novelty cells” in the mouse hippocampal CA1 area that belong to a family of vasoactive intestinal polypeptide-expressing interneurons (VIP-INs). In freely behaving mice, VIP-INs become highly active during spatial exploration in novel environments, enabling rapid encoding of spatial information and regulating the recognition memory.
In the CA1 hippocampus, vasoactive intestinal polypeptide-expressing interneurons (VIP-INs) play a prominent role in disinhibitory circuit motifs. However, the specific behavioral conditions that lead to circuit disinhibition remain uncertain. To investigate the behavioral relevance of VIP-IN activity, we employed wireless technologies allowing us to monitor and manipulate their function in freely behaving mice. Our findings reveal that, during spatial exploration in new environments, VIP-INs in the CA1 hippocampal region become highly active, facilitating the rapid encoding of novel spatial information. Remarkably, both VIP-INs and pyramidal neurons (PNs) exhibit increased activity when encountering novel changes in the environment, including context- and object-related alterations. Concurrently, somatostatin- and parvalbumin-expressing inhibitory populations show an inverse relationship with VIP-IN and PN activity, revealing circuit disinhibition that occurs on a timescale of seconds. Thus, VIP-IN-mediated disinhibition may constitute a crucial element in the rapid encoding of novelty and the acquisition of recognition memory.
ArticleNumber 114115
Author Topolnik, Lisa
Singh, Sanjay
El Amine Barkat, Mohamed
Guet-McCreight, Alexandre
Topolnik, Dimitry
Tamboli, Suhel
Radhakrishnan, Risna
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  fullname: Topolnik, Lisa
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  organization: Neuroscience Axis, CRCHUQ-CHUL, Quebec City, PQ, Canada
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Snippet In the CA1 hippocampus, vasoactive intestinal polypeptide-expressing interneurons (VIP-INs) play a prominent role in disinhibitory circuit motifs. However, the...
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SubjectTerms Animals
CA1 Region, Hippocampal - cytology
CA1 Region, Hippocampal - metabolism
CA1 Region, Hippocampal - physiology
CP: Neuroscience
Exploratory Behavior - physiology
Interneurons - metabolism
Interneurons - physiology
Male
Memory - physiology
Mice
Mice, Inbred C57BL
Parvalbumins - metabolism
Pyramidal Cells - metabolism
Pyramidal Cells - physiology
Recognition, Psychology - physiology
Somatostatin - metabolism
Vasoactive Intestinal Peptide - metabolism
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Title Mouse hippocampal CA1 VIP interneurons detect novelty in the environment and support recognition memory
URI https://dx.doi.org/10.1016/j.celrep.2024.114115
https://www.ncbi.nlm.nih.gov/pubmed/38607918
https://search.proquest.com/docview/3038438347
https://doaj.org/article/0014c5e195b04b84a385ab3d1dcc7df4
Volume 43
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