Spike-Timing-Dependent Plasticity of Neocortical Excitatory Synapses on Inhibitory Interneurons Depends on Target Cell Type

Lu, Juan; Li, Chengyu; Zhao, Jianping; Poo, Mu‐ming; Zhang, Xiao-Hui

doi:10.1523/jneurosci.2513-07.2007

Cited by 148 publications

(173 citation statements)

References 58 publications

Supporting

Mentioning

161

Contrasting

Order By: Relevance

“…1B) could be driven by spike-timing-dependent plasticity in FS interneurons, as postulated previously (10). Coincident (±10 ms) firing between presynaptic principal and postsynaptic FS neurons within the extragranular cortex causes synaptic depression in vitro, regardless of which of the neurons fires first (19). Accordingly, the more active an excitatory input is, the greater the likelihood of both coincident FS postsynaptic activity and synaptic depression in vivo.…”

Section: Md-induced Response Depression In Fs Interneurons Is Consistentmentioning

confidence: 61%

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

View full text Add to dashboard Cite

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 ...

show abstract

Section: Md-induced Response Depression In Fs Interneurons Is Consistentmentioning

confidence: 61%

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

View full text Add to dashboard Cite

show abstract

“…Reduced neuronal activity is likely resulting from a depression of the excitatory inputs. Excitatory synapses at FS inhibitory interneurons largely follow an anti-Hebbian rule of synaptic plasticity (for review, see Kullmann and Lamsa, 2007), showing synaptic LTD after prolonged high-frequency input activity and following repeated application of a spike-time-dependent plasticity stimulation protocol usually inducing LTP in excitatory neurons (Lu et al, 2007). Moreover, brain-derived neurotrophic factor (BDNF) released during high-frequency input activity (Hartmann et al, 2002) promotes synaptic depression at excitatory inputs to PVpositive neurons (Jiang et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Theta-Burst Transcranial Magnetic Stimulation Alters Cortical Inhibition

Benali¹,

Trippe²,

Weiler³

et al. 2011

J. Neurosci.

180

190

View full text Add to dashboard Cite

Human cortical excitability can be modified by repetitive transcranial magnetic stimulation (rTMS), but the cellular mechanisms are largely unknown. Here, we show that the pattern of delivery of theta-burst stimulation (TBS) (continuous versus intermittent) differently modifies electric activity and protein expression in the rat neocortex. Intermittent TBS (iTBS), but not continuous TBS (cTBS), enhanced spontaneous neuronal firing and EEG gamma band power. Sensory evoked cortical inhibition increased only after iTBS, although both TBS protocols increased the first sensory response arising from the resting cortical state. Changes in the cortical expression of the calcium-binding proteins parvalbumin (PV) and calbindin D-28k (CB) indicate that changes in spontaneous and evoked cortical activity following rTMS are in part related to altered activity of inhibitory systems. By reducing PV expression in the fast-spiking interneurons, iTBS primarily affected the inhibitory control of pyramidal cell output activity, while cTBS, by reducing CB expression, more likely affected the dendritic integration of synaptic inputs controlled by other classes of inhibitory interneurons. Calretinin, the third major calcium-binding protein expressed by another class of interneurons was not affected at all. We conclude that different patterns of TBS modulate the activity of inhibitory cell classes differently, probably depending on the synaptic connectivity and the preferred discharge pattern of these inhibitory neurons.

show abstract

“…Since c-Fos expression appears to reflect the activity level but not the activity pattern of neurons, direct measurement of the activity pattern of callosal projection neurons, by electrophysiological recordings, for example, may be required to assess their rhythmic activity. A previous study has shown that the activity of SST-positive cells appears to be blocked by NMDA receptor antagonists more easily than the activity of PV-positive interneurons (Lu et al, 2007) Mechanisms by which MGE cell transplantation prevents PCP-induced behavioral deficits It remains unclear how MGE cell transplantation prevented PCPinduced behavioral deficits. Although we found that the preventive effect of MGE cell transplantation on the PCP-induced behavioral deficits was accompanied by an increase in the c-Fos level in the mPFC (Fig.…”

Section: Mge Cell Transplantation Did Not Cause Behavioral Effects Inmentioning

confidence: 99%

GABAergic Precursor Transplantation into the Prefrontal Cortex Prevents Phencyclidine-Induced Cognitive Deficits

Tanaka

Toriumi

Kubo³

et al. 2011

J. Neurosci.

View full text Add to dashboard Cite

Phencyclidine (PCP) is a noncompetitive NMDA receptor antagonist, and it induces schizophreniform cognitive deficits in healthy humans and similar cognitive deficits in rodents. Although the PCP-induced cognitive deficits appear to be accompanied and possibly caused by dysfunction of GABAergic inhibitory interneurons in the prefrontal cortex (PFC), the potential benefit(s) of GABAergic interneuron manipulations on PCP-induced cognitive deficits remains unexplored. In this study we show that when embryonic medial ganglionic eminence (MGE) cells, many of which differentiate into cortical GABAergic interneurons in situ, were grafted into the medial PFC (mPFC) of neonatal mice, they differentiated into a specific class of GABAergic interneurons and became functionally integrated into the host neuronal circuitry in adults. Prior MGE cell transplantation into the mPFC significantly prevented the induction of cognitive and sensory-motor gating deficits by PCP. The preventive effects were not reproduced by either transplantation of cortical projection neuron precursors into the mPFC or transplantation of MGE cells into the occipital cortex. The preventive effects of MGE cell transplantation into the mPFC were accompanied by activation of callosal projection neurons in the mPFC. These findings suggest that increasing GABAergic interneuron precursors in the PFC may contribute to the development of a cell-based approach as a novel means of modulating the PFC neuronal circuitry and preventing schizophreniform cognitive deficits.

show abstract

Spike-Timing-Dependent Plasticity of Neocortical Excitatory Synapses on Inhibitory Interneurons Depends on Target Cell Type

Cited by 148 publications

References 58 publications

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

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

Theta-Burst Transcranial Magnetic Stimulation Alters Cortical Inhibition

GABAergic Precursor Transplantation into the Prefrontal Cortex Prevents Phencyclidine-Induced Cognitive Deficits

Contact Info

Product

Resources

About