Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus

Summary: Synchronized activity is a universal characteristic of immature neural circuits that is essential for their developmental refinement and strongly depends on GABAergic neurotransmission. A major subpopulation of GABA-releasing interneurons (INs) expresses somatostatin (SOM) and proved critic...

Full description

Bibliographic Details
Main Authors: Tom Flossmann, Thomas Kaas, Vahid Rahmati, Stefan J. Kiebel, Otto W. Witte, Knut Holthoff, Knut Kirmse
Format: Article
Language:English
Published: Elsevier 2019-03-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124719302402
id doaj-474b97f01b864a13990801356f936d6d
record_format Article
spelling doaj-474b97f01b864a13990801356f936d6d2020-11-25T00:17:51ZengElsevierCell Reports2211-12472019-03-01261231733182.e5Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal HippocampusTom Flossmann0Thomas Kaas1Vahid Rahmati2Stefan J. Kiebel3Otto W. Witte4Knut Holthoff5Knut Kirmse6Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, GermanyHans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, GermanyDepartment of Psychology, Technische Universität Dresden, 01187 Dresden, GermanyDepartment of Psychology, Technische Universität Dresden, 01187 Dresden, GermanyHans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, GermanyHans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, GermanyHans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany; Corresponding authorSummary: Synchronized activity is a universal characteristic of immature neural circuits that is essential for their developmental refinement and strongly depends on GABAergic neurotransmission. A major subpopulation of GABA-releasing interneurons (INs) expresses somatostatin (SOM) and proved critical for rhythm generation in adulthood. Here, we report a mechanism whereby SOM INs promote neuronal synchrony in the neonatal CA1 region. Combining imaging and electrophysiological approaches, we demonstrate that SOM INs and pyramidal cells (PCs) coactivate during spontaneous activity. Bidirectional optogenetic manipulations reveal excitatory GABAergic outputs to PCs that evoke correlated network events in an NKCC1-dependent manner and contribute to spontaneous synchrony. Using a dynamic systems modeling approach, we show that SOM INs affect network dynamics through a modulation of network instability and amplification threshold. Our study identifies a network function of SOM INs with implications for the activity-dependent construction of developing brain circuits. : Developing neural circuits generate burst-like spontaneous activity. Flossmann et al. report a mechanism whereby somatostatin interneurons promote neuronal synchrony in the neonatal hippocampus. This action depends on depolarizing GABAergic output synapses and requires chloride uptake via NKCC1. Their findings have implications for the activity-dependent refinement of developing brain circuits. Keywords: GABA, interneurons, development, hippocampus, optogeneticshttp://www.sciencedirect.com/science/article/pii/S2211124719302402
collection DOAJ
language English
format Article
sources DOAJ
author Tom Flossmann
Thomas Kaas
Vahid Rahmati
Stefan J. Kiebel
Otto W. Witte
Knut Holthoff
Knut Kirmse
spellingShingle Tom Flossmann
Thomas Kaas
Vahid Rahmati
Stefan J. Kiebel
Otto W. Witte
Knut Holthoff
Knut Kirmse
Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
Cell Reports
author_facet Tom Flossmann
Thomas Kaas
Vahid Rahmati
Stefan J. Kiebel
Otto W. Witte
Knut Holthoff
Knut Kirmse
author_sort Tom Flossmann
title Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
title_short Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
title_full Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
title_fullStr Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
title_full_unstemmed Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus
title_sort somatostatin interneurons promote neuronal synchrony in the neonatal hippocampus
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2019-03-01
description Summary: Synchronized activity is a universal characteristic of immature neural circuits that is essential for their developmental refinement and strongly depends on GABAergic neurotransmission. A major subpopulation of GABA-releasing interneurons (INs) expresses somatostatin (SOM) and proved critical for rhythm generation in adulthood. Here, we report a mechanism whereby SOM INs promote neuronal synchrony in the neonatal CA1 region. Combining imaging and electrophysiological approaches, we demonstrate that SOM INs and pyramidal cells (PCs) coactivate during spontaneous activity. Bidirectional optogenetic manipulations reveal excitatory GABAergic outputs to PCs that evoke correlated network events in an NKCC1-dependent manner and contribute to spontaneous synchrony. Using a dynamic systems modeling approach, we show that SOM INs affect network dynamics through a modulation of network instability and amplification threshold. Our study identifies a network function of SOM INs with implications for the activity-dependent construction of developing brain circuits. : Developing neural circuits generate burst-like spontaneous activity. Flossmann et al. report a mechanism whereby somatostatin interneurons promote neuronal synchrony in the neonatal hippocampus. This action depends on depolarizing GABAergic output synapses and requires chloride uptake via NKCC1. Their findings have implications for the activity-dependent refinement of developing brain circuits. Keywords: GABA, interneurons, development, hippocampus, optogenetics
url http://www.sciencedirect.com/science/article/pii/S2211124719302402
work_keys_str_mv AT tomflossmann somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT thomaskaas somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT vahidrahmati somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT stefanjkiebel somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT ottowwitte somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT knutholthoff somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
AT knutkirmse somatostatininterneuronspromoteneuronalsynchronyintheneonatalhippocampus
_version_ 1725377898890657792