Alternating sources of perisomatic inhibition during behavior

Dudok, Barna; Klein, Peter; Hwaun, Ernie; Lee, Brian; Yao, Zizhen; Fong, Olivia; Bowler, John C; Terada, Satoshi; Sparks, Fraser T.; Szabó, Gergely; Farrell, Jordan S.; Berg, Jim; Daigle, Tanya L.; Tasic, Bosiljka; Dimidschstein, Jordane; Fishell, Gord; Losonczy, Attila; Zeng, Hongkui; Soltész, Iván

doi:10.1016/j.neuron.2021.01.003

Cited by 97 publications

(133 citation statements)

References 90 publications

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“…PV+ BCs in the hippocampus have been shown to be modulated by CCK (Lee et al, 2011) which would have very interesting implications for the effect of SuM activity in area CA2. Furthermore, it was recently shown that PV+ BCs actively inhibit CCK+ BCs, enabling a complementary perisomatic inhibitory system that allows for brain-state dependent activity during behavior (Dudok et al, 2021) Recent studies have indicated that the SuM input to CA2 plays a key role in social novelty discrimination (Chen et al, 2020). Our findings are very consistent with the finding that DORmediated inhibitory synaptic plasticity of PV+ INs in area CA2 is required for social recognition memory (Domínguez et al, 2019).…”

Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

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Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

Robert

Therreau

Chevaleyre

et al. 2021

eLife

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The hippocampus is critical for memory formation. The hypothalamic supramammillary nucleus (SuM) sends long-range projections to hippocampal area CA2. While the SuM-CA2 connection is critical for social memory, how this input acts on the local circuit is unknown. Using mice, we found that SuM axon stimulation elicited mixed excitatory and inhibitory responses in area CA2 pyramidal neurons (PNs). Parvalbumin-expressing basket cells were largely responsible for the feedforward inhibitory drive of SuM over area CA2. Inhibition recruited by the SuM input onto CA2 PNs increased the precision of action potential firing both in conditions of low and high cholinergic tone. Furthermore, SuM stimulation in area CA2 modulated CA1 activity, indicating that synchronized CA2 output drives a pulsed inhibition in area CA1. Hence, the network revealed here lays basis for understanding how SuM activity directly acts on the local hippocampal circuit to allow social memory encoding.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

Robert

Therreau

Chevaleyre

et al. 2021

eLife

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“…Other reporter lines ( 5HT3AR EGFP ) target the entire CGE-derived interneuron population, of which CCK+ INs only comprise ~ 10% [ 113 , 114 ]. A recently developed Sncg FlpO mouse line appears to provide selective genetic access CCK+ basket cells by taking advantage of the fact that Sncg is specifically expressed in CCK+ INs [ 115 ]. However, it is not clear when the onset of recombination occurs in this line, and whether it will be useful for studying the early development of CCK+ INs.…”

Section: Discussionmentioning

confidence: 99%

Neuronal Dystroglycan regulates postnatal development of CCK/cannabinoid receptor-1 interneurons

Miller

Wright

2021

Neural Dev

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Background The development of functional neural circuits requires the precise formation of synaptic connections between diverse neuronal populations. The molecular pathways that allow GABAergic interneuron subtypes in the mammalian brain to initially recognize their postsynaptic partners remain largely unknown. The transmembrane glycoprotein Dystroglycan is localized to inhibitory synapses in pyramidal neurons, where it is required for the proper function of CCK+ interneurons. However, the precise temporal requirement for Dystroglycan during inhibitory synapse development has not been examined. Methods In this study, we use NEXCre or Camk2aCreERT2 to conditionally delete Dystroglycan from newly-born or adult pyramidal neurons, respectively. We then analyze forebrain development from postnatal day 3 through adulthood, with a particular focus on CCK+ interneurons. Results In the absence of postsynaptic Dystroglycan in developing pyramidal neurons, presynaptic CCK+ interneurons fail to elaborate their axons and largely disappear from the cortex, hippocampus, amygdala, and olfactory bulb during the first two postnatal weeks. Other interneuron subtypes are unaffected, indicating that CCK+ interneurons are unique in their requirement for postsynaptic Dystroglycan. Dystroglycan does not appear to be required in adult pyramidal neurons to maintain CCK+ interneurons. Bax deletion did not rescue CCK+ interneurons in Dystroglycan mutants during development, suggesting that they are not eliminated by canonical apoptosis. Rather, we observed increased innervation of the striatum, suggesting that the few remaining CCK+ interneurons re-directed their axons to neighboring areas where Dystroglycan expression remained intact. Conclusion Together these findings show that Dystroglycan functions as part of a synaptic partner recognition complex that is required early for CCK+ interneuron development in the forebrain.

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“…One possibility is that optical suppression of PV-INs disinhibits a subset of non-PV interneurons which increase firing and compensate for the loss of PV-IN mediated inhibition. In this regard, the reciprocal activity states of PV and CCK neurons, recently reported in CA1, suggests that such a compensation is possible (Dudok et al, 2021). However, whether such a mechanism would exactly compensate for the reduction in PV-IN mediated IPSCs in a slice is debatable.…”

Section: Discussionmentioning

confidence: 99%

Differential Activity-Dependent Increase in Synaptic Inhibition and Parvalbumin Interneuron Recruitment in Dentate Granule Cells and Semilunar Granule Cells

Afrasiabi

Gupta

et al. 2021

Preprint

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Strong inhibitory synaptic gating of dentate gyrus granule cells (GCs), attributed largely to fast-spiking parvalbumin interneurons (PV-INs), is essential to maintain sparse network activity needed for dentate dependent behaviors. However, the contribution of PV-INs to basal and input driven sustained synaptic inhibition in GCs and semilunar granule cells (SGCs), a sparse morphologically distinct dentate projection neuron subtype are currently unknown. We find that although basal inhibitory postsynaptic currents (IPSCs) are more frequent in SGCs and optical activation of PV-INs elicited IPSCs in both GCs and SGCs, optical suppression of PV-INs failed to reduce IPSC frequency in either cell type. Amplitude and kinetics of IPSCs evoked by perforant path activation were not different between GCs and SGCs. However, the robust increase in sustained polysynaptic IPSCs elicited by paired afferent stimulation was lower in SGCs than in simultaneously recorded GCs. Optical suppression of PV-IN selectively reduced sustained IPSCs in SGCs but not in GCs. These results demonstrate that PV-INs, while contributing minimally to basal synaptic inhibition in both GCs and SGCs in slices, mediate sustained feedback inhibition selectively in SGCs. The temporally selective blunting of activity-driven sustained inhibitory gating of SGCs could support their preferential and persistent recruitment during behavioral tasks.

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Alternating sources of perisomatic inhibition during behavior

Cited by 97 publications

References 90 publications

Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

Neuronal Dystroglycan regulates postnatal development of CCK/cannabinoid receptor-1 interneurons

Differential Activity-Dependent Increase in Synaptic Inhibition and Parvalbumin Interneuron Recruitment in Dentate Granule Cells and Semilunar Granule Cells

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