Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency

Amilhon, Bénédicte; Huh, Carey Y. L.; Manseau, Frédéric; Ducharme, Guillaume; Nichol, Heather; Adamantidis, Antoine; Williams, Sylvain

doi:10.1016/j.neuron.2015.05.027

Cited by 222 publications

(257 citation statements)

References 40 publications

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“…These inhibitory neurons expressing PV and SOM, among the most affected populations impacted by aging in the hippocampus (26,27,31,59,60), have been shown to play important roles in learning and memory operations (28)(29)(30)(31)61). As our memory-guided learning task plausibly engages hippocampal processes, the positive changes recorded in inhibitory neuronal populations presumably reflect the fact that our simple form of training has induced physical and functional changes that have had positive, generalized impacts expressed very broadly across forebrain networks.…”

Section: Discussionmentioning

confidence: 91%

Positive impacts of early auditory training on cortical processing at an older age

Cheng

Jia

Zhang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Progressive negative behavioral changes in normal aging are paralleled by a complex series of physical and functional declines expressed in the cerebral cortex. In studies conducted in the auditory domain, these degrading physical and functional cortical changes have been shown to be broadly reversed by intensive progressive training that improves the spectral and temporal resolution of acoustic inputs and suppresses behavioral distractors. Here we found older rats that were intensively trained on an attentionally demanding modulation-rate recognition task in young adulthood substantially retained training-driven improvements in temporal rate discrimination abilities over a subsequent 18-mo epoch-that is, forward into their older age. In parallel, this young-adult auditory training enduringly enhanced temporal and spectral information processing in their primary auditory cortices (A1). Substantially greater numbers of parvalbumin-and somatostatin-labeled inhibitory neurons (closer to the numbers recorded in young vigorous adults) were recorded in the A1 and hippocampus in old trained versus untrained age-matched rats. These results show that a simple form of training in young adulthood in this rat model enduringly delays the otherwise expected deterioration of the physical status and functional operations of the auditory nervous system, with evident training impacts generalized to the hippocampus.aging | auditory cortex | behavioral training | cortical processing | inhibition A degradation of the status of physical brain machinery, expressed by a decline in its temporal processing abilities, has been repeatedly associated with its deteriorating functional status in normal aging (1-4). Recent studies have shown that the machinery that supports processing accuracy and speed, as well as the processes supporting attention control and distractor suppression, can be substantially rejuvenated via simple forms of intensive training in the aged-rat model (4, 5). With auditory perceptual training, in parallel with recovery in behavioral abilities to that matching young-animal performance levels, serials of key physical, chemical, and functional aspects of cortical processing machinery in the trained rats were shown to be restored to a physical or functional status that approached that normally recorded in vigorous young-adult animals.In human studies, substantial changes in speed of processing (SOP) and in other spectro-temporal (or spatiotemporal) signal resolution of performance abilities have been shown to result from attention-demanding, speed-challenged auditory (3, 5-7) or visual training (8-11). For example, the accurate behavioral identification and stimulus-order reconstruction of rapidly successive auditory stimuli was restored in human individuals trained in their eighth decade of life to a performance level normally typifying human performance abilities recorded in their third or fourth decade (3, 6).Our goal here was to define the magnitude and endurance of an intense dose of attention-demanding modulation di...

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Section: Discussionmentioning

confidence: 91%

Positive impacts of early auditory training on cortical processing at an older age

Cheng

Jia

Zhang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The firing of action currents in mouse hippocampal neurons was greatly increased upon CNO exposure. As most of these PV-positive interneurons are GABAergic interneurons (GABA, γ-aminobutyric acid) [2], it is possible that activation of these inhibitory neurons may yield increased inhibition in activity of excitatory neurons in the DG [49-51]. Indeed, hM3D-Gq was expressed in PV-positive neurons in Cre-mice that received lentiviral injection and CNO administration.…”

Section: Discussionmentioning

confidence: 99%

DREADD in Parvalbumin Interneurons of the Dentate Gyrus Modulates Anxiety, Social Interaction and Memory Extinction

Zou

Chen

Deng

et al. 2016

CMM

105

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Parvalbumin (PV)-positive interneurons in the hippocampus play a critical role in animal memory, such as spatial working memory. However, how PV-positive interneurons in the subregions of the hippocampus affect animal behaviors remains poorly defined. Here, we achieved specific and reversible activation of PV-positive interneurons using designer receptors exclusively activated by designer drugs (DREADD) technology. Inducible DREADD expression was demonstrated in vitro in cultured neurons, in which co-transfection of the hM3D-Gq-mCherry vector with a Cre plasmid resulted in a cellular response to hM3Dq ligand clozapine-N-oxide (CNO) stimulation. In addition, the dentate gyrus (DG) of PV-Cre mice received bilateral injection of control lentivirus or lentivirus expressing double floxed hM3D-Gq-mCherry. Selective activation of PV-positive interneurons in the DG did not affect locomotor activity or depression-related behavior in mice. Interestingly, stimulation of PV-positive interneurons induced an anxiolytic effect. Activation of PV-positive interneurons appears to impair social interaction to novelty, but has no effect on social motivation. However, this defect is likely due to the anxiolytic effect as the exploratory behavior of mice expressing hM3D-Gq is significantly increased. Mice expressing hM3D-Gq did not affect novel object recognition. Activation of PV-positive interneurons in the DG maintains intact cued and contextual fear memory but facilitates fear extinction. Collectively, our results demonstrated that proper control of PV interneurons activity in the DG is critical for regulation of the anxiety, social interaction and fear extinction. These results improve our fundamental understanding of the physiological role of PV-positive interneurons in the hippocampus.

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“…Nevertheless, KA elicited a significant decrease in neuronal density in calpain-1 KO mice, suggesting perhaps that the restricted activation of calpain-1 in WT mice in parvalbumin-containing interneurons, and to a lesser extent in CCK-containing interneurons, could nevertheless be involved in the neuroprotection of CA1 and CA3 neurons. It has recently been reported that parvalbumin-containing interneurons are critical for pyramidal cell synchronization of firing and the emergence of hippocampal theta rhythm (Amilhon et al, 2015). It is tempting to speculate that, by protecting these interneurons from KA-mediated neurodegeneration, calpain-1 activation maintains a sufficient degree of inhibition throughout the hippocampal circuitry to limit the extent of neurodegeneration in the pyramidal cells they innervate.…”

Section: Discussionmentioning

confidence: 99%

Differential Activation of Calpain-1 and Calpain-2 following Kainate-Induced Seizure Activity in Rats and Mice

Seinfeld

Baudry

et al. 2016

eneuro

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Visual AbstractSystemic injection of kainate produces repetitive seizure activity in both rats and mice.It also results in short-term synaptic modifications as well as delayed neurodegeneration. The signaling cascades involved in both short-term and delayed responses are not clearly defined. The calcium-dependent protease calpain is activated in various brain structures following systemic kainate injection, although the precise involvement of the two major brain calpain isoforms, calpain-1 and calpain-2, remains to be defined. It has recently been reported that calpain-1 and calpain-2 play opposite roles in NMDA receptor-mediated neuroprotection or neurode- Significance StatementSeizure activity results in both short-term and long-term alterations in the structure and organization of neurons in hippocampus. While the activation of calpain has been well documented following kainic acid (KA)-induced seizures, there is no information regarding the roles of the two major calpain isoforms in the brain, calpain-1 and calpain-2, in the consequences of seizures. Here we report the surprising findings that, while calpain-2 is rapidly activated in all pyramidal cells of CA1 and CA3, calpain-1 activation is restricted to a small population of interneurons following systemic KA injection. Furthermore, KA-induced neurodegeneration in CA1 is exacerbated in calpain-1 knock-out mice, further supporting the notion that calpain-1 is neuroprotective and calpain-2 is neurodegenerative. New ResearchJuly/August 2016, 3(4) e0088-15.2016 1-12 generation, with calpain-1 being neuroprotective and calpain-2 being neurodegenerative. In the present study, we determined the activation pattern of calpain-1 and calpain-2 by analyzing changes in levels of different calpain substrates, including spectrin, drebrin, and PTEN (phosphatase and tensin homolog; a specific calpain-2 substrate) in both rats, and wild-type and calpain-1 knock-out mice. The results indicate that, while calpain-2 is rapidly activated in pyramidal cells throughout CA1 and CA3, rapid calpain-1 activation is restricted to parvalbumin-positive and to a lesser extent CCKpositive, but not somatostatin-positive, interneurons. In addition, calpain-1 knock-out mice exhibit increased long-term neurodegeneration in CA1, reinforcing the notion that calpain-1 activation is neuroprotective.

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Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency

Cited by 222 publications

References 40 publications

Positive impacts of early auditory training on cortical processing at an older age

Positive impacts of early auditory training on cortical processing at an older age

DREADD in Parvalbumin Interneurons of the Dentate Gyrus Modulates Anxiety, Social Interaction and Memory Extinction

Differential Activation of Calpain-1 and Calpain-2 following Kainate-Induced Seizure Activity in Rats and Mice

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