Subfield-Specific Interneuron Circuits Govern the Hippocampal Response to Novelty

Hainmueller, Thomas; Huang, Liwen; Bartos, Marlene

doi:10.2139/ssrn.3796495

Cited by 2 publications

(4 citation statements)

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“…Different hippocampal interneurons show different activity profiles related to locomotion (Lapray et al, 2012; Katona et al, 2014; Arriaga and Han, 2017; Hainmueller et al, 2024). For example, parvalbumin+ (PV) basket and axoaxonic cells, Type 3 interneuron selective interneurons (ISI), and early-born GABAergic ‘hub’ cells have been shown to be more active during movement (Bocchio et al, 2020; Luo et al, 2020; Dudok et al, 2021a, 2021b).…”

Section: Resultsmentioning

confidence: 99%

“…The majority of CA1 interneurons show significant modulation across locomotor states (Fox and Ranck, 1975; Colom and Bland, 1987; Mizumori et al, 1990; Arriaga and Han, 2017; Szabo et al, 2022), with neurogliaform/Ivy cells being a notable exception (Fuentealba et al, 2008; Lapray et al, 2012; Geiller et al, 2020). Of those modulated by locomotion, the majority are positively modulated (Lapray et al, 2012; Geiller et al, 2020; Dudok et al, 2021b; Hainmueller et al, 2024). However, certain populations, including CCK-basket cells, M2R-expressing TORO (theta-off ripple-on) cells, and long-range projecting VIP cells have been shown to have higher activity during rest (Francavilla et al, 2018; Geiller et al, 2020; Dudok et al, 2021a; Szabo et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Within the hippocampus, this circuitry includes inhibitory interneurons (Freund and Buzsaki, 1996), which show a rich diversity of distinct activity profiles during different brain states and behaviors (e.g. (McNaughton et al, 1983; Colom and Bland, 1987; Mizumori et al, 1990; Katona et al, 2014, 2017; Lee et al, 2014; Varga et al, 2014; Arriaga and Han, 2017; Francavilla et al, 2018; Bocchio et al, 2020; Dudok et al, 2021a, 2021b; Szabo et al, 2022; Hainmueller et al, 2024). Hippocampal interneurons can profoundly impact local circuit function, including the formation of CA1 place fields (Grienberger et al, 2017; Dudok et al, 2021b).…”

Section: Introductionmentioning

confidence: 99%

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Distinct functional classes of CA1 hippocampal interneurons are modulated by cerebellar stimulation in a coordinated manner

Froula,

Rose,

Krook-Magnuson

et al. 2024

Preprint

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There is mounting evidence that the cerebellum impacts hippocampal functioning, but the impact of the cerebellum on hippocampal interneurons remains obscure. Using miniscopes in freely behaving animals, we find optogenetic stimulation of Purkinje cells alters the calcium activity of a large percentage of CA1 interneurons. This includes both increases and decreases in activity. Remarkably, this bidirectional impact occurs in a coordinated fashion, in line with interneurons' functional properties. Specifically, CA1 interneurons activated by cerebellar stimulation are commonly locomotion-active, while those inhibited by cerebellar stimulation are commonly rest-active interneurons. We additionally find that subsets of CA1 interneurons show altered activity during object investigations, suggesting a role in the processing of objects in space. Importantly, these neurons also show coordinated modulation by cerebellar stimulation: CA1 interneurons that are activated by cerebellar stimulation are more likely to be activated, rather than inhibited, during object investigations, while interneurons that show decreased activity during cerebellar stimulation show the opposite profile. Therefore, CA1 interneurons play a role in object processing and in cerebellar impacts on the hippocampus, providing insight into previously noted altered CA1 processing of objects in space with cerebellar stimulation. We examined two different stimulation locations (IV/V Vermis; Simplex) and two different stimulation approaches (7Hz or a single 1s light pulse) - in all cases, the cerebellum induces similar coordinated CA1 interneuron changes congruent with an explorative state. Overall, our data show that the cerebellum impacts CA1 interneurons in a bidirectional and coordinated fashion, positioning them to play an important role in cerebello-hippocampal communication.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Distinct functional classes of CA1 hippocampal interneurons are modulated by cerebellar stimulation in a coordinated manner

Froula,

Rose,

Krook-Magnuson

et al. 2024

Preprint

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“…Specifically, INs in the Df(16)A +/mice carry significantly less spatial information (Figs. 2, 4), implicating a decrease in spatially localized inhibitory influence over CA1 pyramidal cell ensembles 71,75,[91][92][93][94][95] . Interestingly, positive place field detection in INs was decreased while negative place fields were preserved, suggesting differential roles for dynamic IN activity.…”

Section: Discussionmentioning

confidence: 99%

Disorganized Inhibitory Dynamics and Functional Connectivity in Hippocampal area CA1 of 22q11.2 Deletion Mutant Mice

Herrlinger,

Rao,

Conde Paredes

et al. 2024

Preprint

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Individuals with the 22q11.2 deletion syndrome, one of the strongest genetic risk factors for schizophrenia, demonstrate cognitive impairments such as episodic memory dysfunction. Place cell dynamics in the hippocampus supporting episodic memory are also impaired in a mouse model for the 22q11.2 deletion (Df(16)A+/-). While hippocampal neural dynamics are under strong inhibitory control, there is no available information about functional alterations of molecularly identified inhibitory circuits in mouse models for the 22q11.2 deletion. Here, we examined interneuron subtype-specific activity dynamics in hippocampal area CA1 of Df(16)A+/- mice performing random foraging and goal-oriented reward learning tasks. We found that Df(16)A+/- inhibitory interneurons carry markedly reduced spatial information during random foraging. Mutant mice perseverate at rewarded locations during reward learning, and multiple interneuron types exhibit aberrant responses to reward locations. We observe task-dependent changes in relational activity among multiple GABAergic subtypes, suggesting a broadly disorganized microcircuit functional connectivity in mutant mice. Overall, we identify widespread and heterogeneous subtype-specific alterations in interneuron dynamics during learning, depicting an inflexible microcircuitry in CA1. Our study provides novel biological insights into how schizophrenia-risk mutations affect local-circuit interactions among diverse cell types in the mouse hippocampus during learning.

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Subfield-Specific Interneuron Circuits Govern the Hippocampal Response to Novelty

Cited by 2 publications

References 0 publications

Distinct functional classes of CA1 hippocampal interneurons are modulated by cerebellar stimulation in a coordinated manner

Distinct functional classes of CA1 hippocampal interneurons are modulated by cerebellar stimulation in a coordinated manner

Disorganized Inhibitory Dynamics and Functional Connectivity in Hippocampal area CA1 of 22q11.2 Deletion Mutant Mice

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