State-Dependent Bidirectional Modification of Somatic Inhibition in Neocortical Pyramidal Cells

Kurotani, Tohru; Yamada, Kazumasa; Yoshimura, Yumiko; Crair, Michael C.; Komatsu, Yukio

doi:10.1016/j.neuron.2008.01.030

Cited by 81 publications

(111 citation statements)

References 59 publications

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“…Recent in vitro study reported state-dependent insertion of GABA A receptors in the pyramidal cells of the rat visual cortex (Kurotani et al, 2008). Thus, state-dependent insertion or modulation of GABA A receptors of the postsynaptic membrane (Gaiarsa et al, 2002;Jacob et al, 2008) of mitral cells might explain our results of state-dependent change of granule-tomitral inhibition.…”

supporting

confidence: 50%

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Tsuno¹,

Kashiwadani²,

Mori³

2008

J. Neurosci.

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Behavioral states regulate how information is processed in local neuronal circuits. Here, we asked whether dendrodendritic synaptic interactions in the olfactory bulb vary with brain and behavioral states. To examine the state-dependent change of the dendrodendritic synaptic transmission, we monitored changes in field potential responses in the olfactory bulb of urethane-anesthetized and freely behaving rats. In urethane-anesthetized rats, granule-to-mitral dendrodendritic synaptic inhibition was larger and longer when slow waves were present in the electroencephalogram (slow-wave state) than during the fast-wave state. The state-dependent alternating change in the granule-to-mitral inhibition was regulated by the cholinergic system. In addition, the frequency of the spontaneous oscillatory activity of local field potentials and periodic discharges of mitral cells in the olfactory bulb shifted in synchrony with shifts in the neocortical brain state. Freely behaving rats showed multilevel changes in dendrodendritic synaptic inhibition that corresponded to diverse behavioral states; the inhibition was the largest during slow-wave sleep state, and successively smaller during light sleep, awake immobility, and awake moving states. These results provide evidence that behavioral state-dependent global changes in cholinergic tone modulate dendrodendritic synaptic inhibition and the information processing mode in the olfactory bulb.

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supporting

confidence: 50%

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Tsuno¹,

Kashiwadani²,

Mori³

2008

J. Neurosci.

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“…Future studies will be needed to assess how MD and subsequent sleep affect postsynaptic currents in principal neurons. Enhancement of postsynaptic GABA receptor signaling has been reported in vitro in response to "sleep-like" patterns of activity (30), but it is unclear whether this finding translates to the natural sleep state or how this change in inhibition affects cortical circuit function.…”

Section: Discussionmentioning

confidence: 99%

Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Aton

Broussard

Dumoulin³

et al. 2013

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

140

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Ocular dominance plasticity in the developing primary visual cortex is initiated by monocular deprivation (MD) and consolidated during subsequent sleep. To clarify how visual experience and sleep affect neuronal activity and plasticity, we continuously recorded extragranular visual cortex fast-spiking (FS) interneurons and putative principal (i.e., excitatory) neurons in freely behaving cats across periods of waking MD and post-MD sleep. Consistent with previous reports in mice, MD induces two related changes in FS interneurons: a response shift in favor of the closed eye and depression of firing. Spike-timing-dependent depression of open-eye-biased principal neuron inputs to FS interneurons may mediate these effects. During post-MD nonrapid eye movement sleep, principal neuron firing increases and becomes more phase-locked to slow wave and spindle oscillations. Ocular dominance (OD) shifts in favor of open-eye stimulation-evident only after post-MD sleep -are proportional to MD-induced changes in FS interneuron activity and to subsequent sleep-associated changes in principal neuron activity. OD shifts are greatest in principal neurons that fire 40-300 ms after neighboring FS interneurons during post-MD slow waves. Based on these data, we propose that MD-induced changes in FS interneurons play an instructive role in ocular dominance plasticity, causing disinhibition among open-eye-biased principal neurons, which drive plasticity throughout the visual cortex during subsequent sleep.period shifts neuronal responses in primary visual cortex in favor of open-eye stimulation. Sleep is essential for consolidating ocular dominance plasticity (ODP) in cat visual cortex (1, 2). Specifically, post-MD sleep is required to potentiate open-eye responses in cortical neurons-a process mediated via intracellular pathways involved in long-term potentiation of glutamatergic synapses (1, 3). However, the changes in network activity (during waking experience and subsequent sleep) that mediate ODP remain unknown.One long-standing hypothesis is that ODP is gated by the balance of excitation and inhibition in the visual cortex during the critical period. This idea is supported by findings that ODP is enhanced either by increasing GABAergic neurotransmission before the critical period (4) or by reducing GABA signaling after the critical period (5-8). It has been suggested that, during the critical period, MD itself alters the balance of excitation and feedback inhibition within the visual cortex by depressing the activity of fast-spiking (FS) interneurons (9, 10). In support of this idea, ODP is first detectable in the extragranular cortical layers [i.e., 2/3, 5, and 6 (11)], where depression of FS interneuron activity has been reported after brief MD. These layers are characterized by abundant reciprocal intralaminar connections between FS interneurons and pyramidal neurons (12, 13). In contrast, in layer 4, where ODP is initially weak or absent (11), connections between FS interneurons and pyramidal neurons can be strengthened by MD ...

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“…This may lead to a synapse-specific proportional reduction of synaptic weights of synchronously firing neurons (Birtoli and Ulrich, 2004;Czarnecki et al, 2007). NREM-sleep-related discharge patterns were also shown to enhance GABAergic synaptic transmission (Kurotani et al, 2008). Together, these processes may contribute to the overall decline in excitability observed during sleep with field potential recordings (Barnes et al, 1977;Vyazovskiy et al, 2008).…”

Section: Functional Implicationsmentioning

confidence: 99%

Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep

Lanté

Toledo-Salas²,

Ondrejčák³

et al. 2011

J. Neurosci.

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There is accumulating evidence that sleep contributes to memory formation and learning, but the underlying cellular mechanisms are incompletely understood. To investigate the impact of sleep on excitatory synaptic transmission, we obtained whole-cell patch-clamp recordings from layer V pyramidal neurons in acute slices of somatosensory cortex of juvenile rats (postnatal days 21-25). In animals after the dark period, philanthotoxin 74 (PhTx)-sensitive calcium-permeable AMPA receptors (CP-AMPARs) accounted for ϳ25% of total EPSP size, and current-voltage (I-V) relationships of the underlying EPSCs showed inward rectification. In contrast, in similar experiments after the light period, EPSPs were PhTx insensitive with linear I-V characteristics, indicating that CP-AMPARs were less abundant. Combined EEG and EMG recordings confirmed that slow-wave sleep-associated delta wave power peaked at the onset of the more quiescent, lights-on phase of the cycle. Subsequently, we show that burst firing, a characteristic action potential discharge mode of layer V pyramidal neurons during slow-wave sleep has a dual impact on synaptic AMPA receptor composition: repetitive burst firing without synaptic stimulation eliminated CP-AMPARs by activating serine/threonine phosphatases. Additionally, repetitive burst-firing paired with EPSPs led to input-specific long-term depression (LTD), affecting Ca 2ϩ impermeable AMPARs via protein kinase C signaling. In agreement with two parallel mechanisms, simple bursts were ineffective after the light period but paired bursts induced robust LTD. In contrast, incremental LTD was generated by both conditioning protocols after the dark cycle. Together, our results demonstrate qualitative changes at neocortical glutamatergic synapses that can be induced by discharge patterns characteristic of non-rapid eye movement sleep.

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State-Dependent Bidirectional Modification of Somatic Inhibition in Neocortical Pyramidal Cells

Cited by 81 publications

References 59 publications

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep

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State-Dependent Bidirectional Modification of Somatic Inhibition in Neocortical Pyramidal Cells

Cited by 81 publications

References 59 publications

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Removal of Synaptic Ca2+-Permeable AMPA Receptors during Sleep

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Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep