Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus

Shinohara, Yuta; Hosoya, Aki; Hirase, Hajime

doi:10.1038/ncomms2658

Cited by 62 publications

(57 citation statements)

References 37 publications

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“…In contrast to excitatory neurons, inhibitory interneurons have multiple phenotypes that vary in morphology, neurochemistry, and physiology, and represent only 20 to 30 % of neurons in the cortex [11]. In addition, inhibitory networks play a key role in the experiencedependent refinement of neural networks that last through the first postnatal 4 weeks [29,30]. In the present study, we show that repeated sevoflurane exposure caused a significantly decreased PV expression.…”

Section: Discussionsupporting

confidence: 44%

“…By contrast, early life stress such as maternal separation leads to a reduction of PVexpression in the PFC and causes subsequent working memory impairments in adolescence [16]. Since activitydependent regulation of gene expression is critical for inhibitory network remodeling through life experiences [29,30], it is possible that beneficial effects of an enriched environment might be related to its ability to enhance neuronal viability or possibly by providing sufficient compensatory inhibition to the overexcited hippocampal circuitry. Finally, our results revealed that there was no colocalization of caspase-3 and PV interneurons, suggesting that caspase-independent pathways may be involved in mediation of the decreased PV expression induced by sevoflurane [35].…”

Section: Discussionmentioning

confidence: 99%

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Repeated Neonatal Sevoflurane Exposure-Induced Developmental Delays of Parvalbumin Interneurons and Cognitive Impairments Are Reversed by Environmental Enrichment

Wang

Sun

et al. 2016

Mol Neurobiol

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Parvalbumin (PV) interneurons are critically involved in the cognitive processes. Based on prior investigations that environmental enrichment reverses impaired cognition after anesthetic exposure, we proposed that environmental enrichment protects PV interneurons and thereby improves sevoflurane-induced cognitive impairments. Six-day-old C57BL/6 male mice were exposed to 3 % sevoflurane or 30 % oxygen/air 2 h daily for 3 days from postnatal day 6 (P6) to P8. The mice were randomly allocated to an enriched environment for 2 h daily between P8 and P90 or a standard environment. Western blotting and immunofluorescence were used for determining PV expression in the prefrontal cortex and hippocampus. In another set of experiments, cognitive tests were assessed by the open field test (P41), Morris water maze test (P54-60), and fear conditioning tests (P42-43 and P89-90). Exposure of neonatal mice to sevoflurane resulted in a reduced freezing response in the contextual test at P43 but not P90. The PV expression in these mice was decreased at P9, P14, P28, and P42, but not at ≥P60. No colocalization of caspase-3 and 5-bromo-2-deoxyuridine or caspase-3 and PV was observed, suggesting that caspase-independent pathways may be involved in the mediation of sevoflurane-induced down-regulation of PV. The sevoflurane-exposed mice that were placed in an enriched environment exhibited normal behavior and had PV interneurons that did not differ from those in the control mice at P42-43. Neonatal sevoflurane exposure induces a reduced freezing response in the contextual test at P43 and developmental delays in PV interneurons in the prefrontal cortex and hippocampus. Placement of the sevoflurane-exposed mice in an enriched environment can prevent these abnormalities.

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Section: Discussionsupporting

confidence: 44%

Section: Discussionmentioning

confidence: 99%

Repeated Neonatal Sevoflurane Exposure-Induced Developmental Delays of Parvalbumin Interneurons and Cognitive Impairments Are Reversed by Environmental Enrichment

Wang

Sun

et al. 2016

Mol Neurobiol

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“…Alternatively, the same result could arise if the left and right CA3 play independent, but equally necessary, roles in the activity required for short-term memory. One such role could relate to gamma oscillations, which have been closely linked to short-term memory (39), and, interestingly, a left-right asymmetry of gamma power was recently reported in the CA1 of the rat hippocampus following environmental enrichment (40).…”

Section: Discussionmentioning

confidence: 99%

Left–right dissociation of hippocampal memory processes in mice

Shipton

El-Gaby

Apergis-Schoute

et al. 2014

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

166

222

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Left-right asymmetries have likely evolved to make optimal use of bilaterian nervous systems; however, little is known about the synaptic and circuit mechanisms that support divergence of function between equivalent structures in each hemisphere. Here we examined whether lateralized hippocampal memory processing is present in mice, where hemispheric asymmetry at the CA3-CA1 pyramidal neuron synapse has recently been demonstrated, with different spine morphology, glutamate receptor content, and synaptic plasticity, depending on whether afferents originate in the left or right CA3. To address this question, we used optogenetics to acutely silence CA3 pyramidal neurons in either the left or right dorsal hippocampus while mice performed hippocampus-dependent memory tasks. We found that unilateral silencing of either the left or right CA3 was sufficient to impair short-term memory. However, a striking asymmetry emerged in long-term memory, wherein only left CA3 silencing impaired performance on an associative spatial long-term memory task, whereas right CA3 silencing had no effect. To explore whether synaptic properties intrinsic to the hippocampus might contribute to this left-right behavioral asymmetry, we investigated the expression of hippocampal long-term potentiation. Following the induction of long-term potentiation by high-frequency electrical stimulation, synapses between CA3 and CA1 pyramidal neurons were strengthened only when presynaptic input originated in the left CA3, confirming an asymmetry in synaptic properties. The dissociation of hippocampal long-term memory function between hemispheres suggests that memory is routed via distinct left-right pathways within the mouse hippocampus, and provides a promising approach to help elucidate the synaptic basis of long-term memory. U nilateral specializations may facilitate greater processing power in bilateral brain structures by using the available neuronal circuitry more effectively. Nevertheless, the nature of the mechanisms that can act within the confines of duplicate neural structures to support different cognitive functions in each hemisphere remains elusive.The hippocampus is essential for certain forms of learning and memory, both in humans (1) and in rodents (2, 3), and also plays an important role in navigation (4). The left and right mammalian hippocampi comprise the same anatomical areas and directional connectivity, and yet in the human hippocampus, taskrelated activity may be localized to only one hemisphere (5). This lateralization may enable the left and right hippocampus to support complementary functions in human episodic memory, with left hippocampal activity associated with an egocentric, sequential representation of space but greater activity in the right hippocampus when an allocentric representation is used (6). It has been suggested that human hippocampal asymmetry is primarily dictated by external asymmetry-namely, the left hemispheric involvement in language processing and the stronger contribution of the right hemisphere to visuosp...

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“…We recently found that hippocampal gamma amplitude increases in rats raised in EE, which hints at a possible link between gamma oscillation and learning [71]. Increases of spine density and dendritic complexity are common effects of EE in the cortex and hippocampus.…”

Section: Neuromodulator Activation and Gamma Oscillationsmentioning

confidence: 99%

Volume transmission signalling via astrocytes

Hirase

Iwai

Takata

et al. 2014

Phil. Trans. R. Soc. B

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The influence of astrocytes on synaptic function has been increasingly studied, owing to the discovery of both gliotransmission and morphological ensheathment of synapses. While astrocytes exhibit at best modest membrane potential fluctuations, activation of G-protein coupled receptors (GPCRs) leads to a prominent elevation of intracellular calcium which has been reported to correlate with gliotransmission. In this review, the possible role of astrocytic GPCR activation is discussed as a trigger to promote synaptic plasticity, by affecting synaptic receptors through gliotransmitters. Moreover, we suggest that volume transmission of neuromodulators could be a biological mechanism to activate astrocytic GPCRs and thereby to switch synaptic networks to the plastic mode during states of attention in cerebral cortical structures.

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Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus

Cited by 62 publications

References 37 publications

Repeated Neonatal Sevoflurane Exposure-Induced Developmental Delays of Parvalbumin Interneurons and Cognitive Impairments Are Reversed by Environmental Enrichment

Repeated Neonatal Sevoflurane Exposure-Induced Developmental Delays of Parvalbumin Interneurons and Cognitive Impairments Are Reversed by Environmental Enrichment

Left–right dissociation of hippocampal memory processes in mice

Volume transmission signalling via astrocytes

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