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Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network
by
Rudolph, Stephanie
, Yap, Ee-Lynn
, Pettit, Noah L.
, Harmin, David A.
, Sharma, Nikhil
, Golden, Emily
, Nagy, M. Aurel
, Harvey, Christopher D.
, Dagliyan, Onur
, Lin, Cindy
, Davis, Christopher P.
, Griffith, Eric C.
, Greenberg, Michael E.
in
13/1
/ 13/106
/ 13/109
/ 13/31
/ 13/51
/ 13/62
/ 13/89
/ 14/19
/ 14/32
/ 14/35
/ 38/109
/ 38/23
/ 38/39
/ 38/90
/ 38/91
/ 42/41
/ 631/378/1595/1554
/ 631/378/1697/1691
/ 631/378/2591
/ 631/378/340
/ 631/378/3920
/ 64/60
/ 82/29
/ 9/30
/ 9/74
/ Animals
/ CA1 Region, Hippocampal - metabolism
/ Cholecystokinin
/ Cholecystokinin - metabolism
/ Chromatin
/ Circuits
/ Electrophysiology
/ Exploratory Behavior - physiology
/ Female
/ Gamma Rhythm
/ Gene sequencing
/ Genes
/ Hippocampus
/ Humanities and Social Sciences
/ Interneurons
/ Interneurons - metabolism
/ Kinases
/ Male
/ Memory Consolidation
/ Mice
/ multidisciplinary
/ Nerve Net - cytology
/ Nerve Net - physiology
/ Neural Inhibition
/ Neuronal Plasticity - physiology
/ Neurons
/ Neuropeptides
/ Parvalbumin
/ Parvalbumins - metabolism
/ Plastic properties
/ Plasticity
/ Predictions
/ Proto-Oncogene Proteins c-fos - metabolism
/ Pyramidal cells
/ Pyramidal Cells - metabolism
/ Science
/ Science (multidisciplinary)
/ Secretogranin II - genetics
/ Secretogranin II - metabolism
/ Spatial Navigation - physiology
/ Theta Rhythm
/ Transcription factors
2021
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Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network
by
Rudolph, Stephanie
, Yap, Ee-Lynn
, Pettit, Noah L.
, Harmin, David A.
, Sharma, Nikhil
, Golden, Emily
, Nagy, M. Aurel
, Harvey, Christopher D.
, Dagliyan, Onur
, Lin, Cindy
, Davis, Christopher P.
, Griffith, Eric C.
, Greenberg, Michael E.
in
13/1
/ 13/106
/ 13/109
/ 13/31
/ 13/51
/ 13/62
/ 13/89
/ 14/19
/ 14/32
/ 14/35
/ 38/109
/ 38/23
/ 38/39
/ 38/90
/ 38/91
/ 42/41
/ 631/378/1595/1554
/ 631/378/1697/1691
/ 631/378/2591
/ 631/378/340
/ 631/378/3920
/ 64/60
/ 82/29
/ 9/30
/ 9/74
/ Animals
/ CA1 Region, Hippocampal - metabolism
/ Cholecystokinin
/ Cholecystokinin - metabolism
/ Chromatin
/ Circuits
/ Electrophysiology
/ Exploratory Behavior - physiology
/ Female
/ Gamma Rhythm
/ Gene sequencing
/ Genes
/ Hippocampus
/ Humanities and Social Sciences
/ Interneurons
/ Interneurons - metabolism
/ Kinases
/ Male
/ Memory Consolidation
/ Mice
/ multidisciplinary
/ Nerve Net - cytology
/ Nerve Net - physiology
/ Neural Inhibition
/ Neuronal Plasticity - physiology
/ Neurons
/ Neuropeptides
/ Parvalbumin
/ Parvalbumins - metabolism
/ Plastic properties
/ Plasticity
/ Predictions
/ Proto-Oncogene Proteins c-fos - metabolism
/ Pyramidal cells
/ Pyramidal Cells - metabolism
/ Science
/ Science (multidisciplinary)
/ Secretogranin II - genetics
/ Secretogranin II - metabolism
/ Spatial Navigation - physiology
/ Theta Rhythm
/ Transcription factors
2021
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Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network
by
Rudolph, Stephanie
, Yap, Ee-Lynn
, Pettit, Noah L.
, Harmin, David A.
, Sharma, Nikhil
, Golden, Emily
, Nagy, M. Aurel
, Harvey, Christopher D.
, Dagliyan, Onur
, Lin, Cindy
, Davis, Christopher P.
, Griffith, Eric C.
, Greenberg, Michael E.
in
13/1
/ 13/106
/ 13/109
/ 13/31
/ 13/51
/ 13/62
/ 13/89
/ 14/19
/ 14/32
/ 14/35
/ 38/109
/ 38/23
/ 38/39
/ 38/90
/ 38/91
/ 42/41
/ 631/378/1595/1554
/ 631/378/1697/1691
/ 631/378/2591
/ 631/378/340
/ 631/378/3920
/ 64/60
/ 82/29
/ 9/30
/ 9/74
/ Animals
/ CA1 Region, Hippocampal - metabolism
/ Cholecystokinin
/ Cholecystokinin - metabolism
/ Chromatin
/ Circuits
/ Electrophysiology
/ Exploratory Behavior - physiology
/ Female
/ Gamma Rhythm
/ Gene sequencing
/ Genes
/ Hippocampus
/ Humanities and Social Sciences
/ Interneurons
/ Interneurons - metabolism
/ Kinases
/ Male
/ Memory Consolidation
/ Mice
/ multidisciplinary
/ Nerve Net - cytology
/ Nerve Net - physiology
/ Neural Inhibition
/ Neuronal Plasticity - physiology
/ Neurons
/ Neuropeptides
/ Parvalbumin
/ Parvalbumins - metabolism
/ Plastic properties
/ Plasticity
/ Predictions
/ Proto-Oncogene Proteins c-fos - metabolism
/ Pyramidal cells
/ Pyramidal Cells - metabolism
/ Science
/ Science (multidisciplinary)
/ Secretogranin II - genetics
/ Secretogranin II - metabolism
/ Spatial Navigation - physiology
/ Theta Rhythm
/ Transcription factors
2021
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Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network
Journal Article
Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network
2021
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Overview
Behavioural experiences activate the FOS transcription factor in sparse populations of neurons that are critical for encoding and recalling specific events
1
–
3
. However, there is limited understanding of the mechanisms by which experience drives circuit reorganization to establish a network of
Fos
-activated cells. It is also not known whether FOS is required in this process beyond serving as a marker of recent neural activity and, if so, which of its many gene targets underlie circuit reorganization. Here we demonstrate that when mice engage in spatial exploration of novel environments, perisomatic inhibition of
Fos
-activated hippocampal CA1 pyramidal neurons by parvalbumin-expressing interneurons is enhanced, whereas perisomatic inhibition by cholecystokinin-expressing interneurons is weakened. This bidirectional modulation of inhibition is abolished when the function of the FOS transcription factor complex is disrupted. Single-cell RNA-sequencing, ribosome-associated mRNA profiling and chromatin analyses, combined with electrophysiology, reveal that FOS activates the transcription of
Scg2
, a gene that encodes multiple distinct neuropeptides, to coordinate these changes in inhibition. As parvalbumin- and cholecystokinin-expressing interneurons mediate distinct features of pyramidal cell activity
4
–
6
, the SCG2-dependent reorganization of inhibitory synaptic input might be predicted to affect network function in vivo. Consistent with this prediction, hippocampal gamma rhythms and pyramidal cell coupling to theta phase are significantly altered in the absence of
Scg2
. These findings reveal an instructive role for FOS and SCG2 in establishing a network of
Fos
-activated neurons via the rewiring of local inhibition to form a selectively modulated state. The opposing plasticity mechanisms acting on distinct inhibitory pathways may support the consolidation of memories over time.
Novel experiences in mice lead to opposing effects on inhibition of
Fos
-activated hippocampal CA1 pyramidal neurons by parvalbumin- and cholecystokinin-expressing interneurons, revealing the roles of FOS and SCG2 in neural plasticity and consolidation of memories.
Publisher
Nature Publishing Group UK,Nature Publishing Group
Subject
/ 13/106
/ 13/109
/ 13/31
/ 13/51
/ 13/62
/ 13/89
/ 14/19
/ 14/32
/ 14/35
/ 38/109
/ 38/23
/ 38/39
/ 38/90
/ 38/91
/ 42/41
/ 64/60
/ 82/29
/ 9/30
/ 9/74
/ Animals
/ CA1 Region, Hippocampal - metabolism
/ Cholecystokinin - metabolism
/ Circuits
/ Exploratory Behavior - physiology
/ Female
/ Genes
/ Humanities and Social Sciences
/ Kinases
/ Male
/ Mice
/ Neuronal Plasticity - physiology
/ Neurons
/ Proto-Oncogene Proteins c-fos - metabolism
/ Pyramidal Cells - metabolism
/ Science
/ Secretogranin II - metabolism
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