Extrinsic control of the early postnatal CA1 hippocampal circuits

Leprince, Erwan; Dard, Robin F; Mortet, Salomé; Filippi, Caroline; Giorgi-Kurz, Marie; Bourboulou, Romain; Lenck-Santini, Pierre-Pascal; Picardo, Michel A.; Bocchio, Marco; Baude, Agnès; Cossart, Rosa

doi:10.1016/j.neuron.2022.12.013

Cited by 8 publications

(10 citation statements)

References 65 publications

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“…This further implies that neither GDPs in vitro nor eSPWs in vivo are sustained by depolarizing GABAergic (Emx1 -) neurons alone, despite their partially excitatory action (Flossmann et al, 2019;Murata and Colonnese, 2020;Graf et al, 2021). In addition, our data are fully compatible with the previous conclusion that somatosensory feedback, in the form of eSPWs, is relayed to CA1 via Emx1 + glutamatergic projections from the entorhinal cortex (Valeeva et al, 2019;Leprince et al, 2023), whereas glutamatergic input from Emx1sources, such as from the ventral midline thalamus (Leprince et al, 2023), modulates rather than sustains synchronized activity in developing CA1. Similar considerations apply to the second postnatal week, when short-lasting events (i.e., eSPWs) had been largely replaced by discontinuous oscillatory LFP activity (Fig.…”

Section: Generative Mechanisms Of Network Bursts In the Developing Ca1supporting

confidence: 91%

“…To examine the efficacy of G i/o protein-coupled chemogenetic silencing during development, we conditionally expressed hM4Di in telencephalic glutamatergic neurons from embryonic stages onward ( Emx1 IREScre ::hM4Di LSL or hM4Di Emx1 mice) (Gorski et al, 2002; Zhu et al, 2016; Graf et al, 2021). Of note, both CA1 pyramidal cells (PCs) and the vast majority of glutamatergic synapses in CA1 are derived from the Emx1 lineage (Sando et al, 2017; Leprince et al, 2023). We first used three-dimensional acousto-optic two-photon Ca 2+ imaging in CA1 stratum pyramidale of acute brain slices to quantify network activity at single-cell resolution at postnatal days (P) 2–5 (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…4A). Of note, most neurons providing glutamatergic input to CA1 are derived from the Emx1 lineage (Sando et al, 2017; Graf et al, 2021; Leprince et al, 2023). We found that, in CA1 PCs recorded from hM4Di Emx1 mice at P2–5, C21 (1 µM) reduced the frequency of mEPSCs from 0.13 ± 0.03 min −1 to 0.05 ± 0.01 min −1 (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To elucidate the learning rules underlying activity-dependent refinements in brain development, research is increasingly utilizing chemogenetic strategies, as they allow neuronal activity to be manipulated in a temporally controlled and cell type-specific manner (Donato et al, 2017; Wong et al, 2018; Murata and Colonnese, 2020; Leighton et al, 2021; Maldonado et al, 2021; Chen et al, 2023; Kostka and Hanganu-Opatz, 2023; Leprince et al, 2023). The most widely used inhibitory chemogenetic actuator is hM4Di, which is based on the human muscarinic M4 receptor employing G i/o signaling for neuronal silencing (Armbruster et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Chemogenetic silencing reveals presynaptic Gi/o protein-mediated inhibition of synchronized activity in the developing hippocampusin vivo

Graf,

Samiee,

Flossmann

et al. 2024

Preprint

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The development of neuronal circuits is an activity-dependent process. Research aimed at deciphering the learning rules governing these developmental refinements is increasingly utilizing a class of chemogenetic tools that employ Gi/o protein signaling (Gi-DREADDs) for neuronal silencing. However, their mechanisms of action and inhibitory efficacy in immature neurons with incompletely developed Gi/o signaling are poorly understood. Here, we analyze the impact of Gi/o signaling on cellular and network excitability in the neonatal hippocampus by expressing the Gi-DREADD hM4Di in telencephalic glutamatergic neurons of neonatal mice of both sexes. Using acousto-optic two-photon Ca2+ imaging, we report that activation of hM4Di leads to a complete arrest of spontaneous synchronized activity in CA1 in vitro. Electrophysiological analyses demonstrate that hM4Di-mediated silencing is not accounted for by changes in intrinsic excitability of CA1 pyramidal cells (PCs). Instead, activation of hM4Di robustly restrains synaptic glutamate release by the first postnatal week, effectively reducing recurrent excitation in CA1. In vivo, inhibition through hM4Di potently suppresses early sharp waves (eSPWs) and discontinuous oscillatory network activity in CA1 of head-fixed mice before eye opening. In summary, hM4Di dampens glutamatergic neurotransmission through a presynaptic mechanism sufficient to terminate spontaneous synchronized activity in the neonatal CA1. Our findings have implications for designing and interpreting experiments utilizing Gi-DREADDs in immature neurons and further point to a potential role of Gi/o-dependent endogenous neuromodulators in activity-dependent hippocampal development.

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Section: Generative Mechanisms Of Network Bursts In the Developing Ca1supporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Chemogenetic silencing reveals presynaptic Gi/o protein-mediated inhibition of synchronized activity in the developing hippocampusin vivo

Graf,

Samiee,

Flossmann

et al. 2024

Preprint

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“…We selected this as our focal region for several reasons. Firstly, CA1 is under the conjunctive influence of both intra- and extra-hippocampal brain regions [13]. The bidirectional projections between CA1 and multiple other areas render it a major functional area of the hippocampus.…”

Section: Introductionmentioning

confidence: 99%

Neuronal Hyperactivity in the Hippocampus during the Early Stage of Streptozotocin-Induced Type 1 Diabetes in Mice

Fang,

Xu,

Zhang

et al. 2023

Neuroendocrinology

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Introduction Cognitive dysfunction due to reduced neuronal transmission in the brain is a major emerging complication in diabetes. However, recent neuroimaging studies have demonstrated non-linear changes including hyperactivity in the hippocampus during the early stage of diabetes. This study aimed to determine the changes in neuronal activity at a single-cell level in hippocampal CA1 pyramidal neurons in the early stage of streptozotocin-induced type 1 diabetes in mice. Methods Whole-cell patch-clamp recordings from acute brain slices were performed in mice over 4 consecutive weeks following the induction of hyperglycaemia using streptozotocin. In addition, microdialysate was collected from CA1 area while the mice were in an arousal state. The concentrations of glutamate and GABA in the microdialysate was then measured using ultra-performance liquid chromatography with mass spectrometry. Results CA1 Neurons in streptozotocin-induced diabetic mice exhibited higher membrane potentials (p = 0.0052), higher frequency of action potentials (p = 0.0052), and higher frequency of spontaneous excitatory post-synaptic currents (p = 0.037) compared with controls during the second week after hyperglycaemia was established. No changes in electrophysiological parameters were observed during the first, the third and the fourth week. Moreover, the diabetic mice had higher extracellular glutamate concentration in CA1 area compared with controls (p = 0.021) during the second week after the initiation of diabetes. No change in the extracellular GABA concentration was observed. Conclusion Our study demonstrated a temporary state of neuronal hyperactivity at the single-cell level in the hippocampal CA1 region during the early stage of diabetes. This neuronal hyperactivity might be related to altered glutamate metabolism and provide clues for future brain-target intervention.

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Olfactory bulb activity shapes the development of entorhinal-hippocampal coupling and associated cognitive abilities

Chen,

Kostka,

Bitzenhofer

et al. 2023

Current Biology

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Extrinsic control of the early postnatal CA1 hippocampal circuits

Cited by 8 publications

References 65 publications

Chemogenetic silencing reveals presynaptic Gi/o protein-mediated inhibition of synchronized activity in the developing hippocampusin vivo

Chemogenetic silencing reveals presynaptic Gi/o protein-mediated inhibition of synchronized activity in the developing hippocampusin vivo

Neuronal Hyperactivity in the Hippocampus during the Early Stage of Streptozotocin-Induced Type 1 Diabetes in Mice

Olfactory bulb activity shapes the development of entorhinal-hippocampal coupling and associated cognitive abilities

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