Delayed plasticity of inhibitory neurons in developing visual cortex

Gandhi, Sunil; Yanagawa, Yuchio; Stryker, Michael P.

doi:10.1073/pnas.0806159105

Cited by 105 publications

(121 citation statements)

References 40 publications

(68 reference statements)

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“…Recently, it has been reported that both types of neurons showed the similar distribution of ODIs in GAD67-GFP knock-in mice at P25, P28, P30, and P35 (Gandhi et al, 2008). This seemingly different result from the present study may reflect the reduction in the GABA content in the brain of GAD67-GFP knock-in mice, although other factors such as different anesthetics are not completely excluded.…”

Section: Binocularity Of Gabaergic Neuronscontrasting

confidence: 55%

“…If GABAergic neurons play such a role in visual cortical plasticity, their binocular responsiveness and modifiability of this property to monocular visual deprivation may be different from those of excitatory neurons. It is rather surprising that the questions of whether the binocular responsiveness and experience-dependent plasticity are different between the two types of neurons remain essentially unanswered, although there was a study using glutamate decarboxylase 67 (GAD67)-green fluorescent protein (GFP) knock-in mice (Gandhi et al, 2008), in which the GABA content in the brain is abnormally low because of destruction of the endogenous GAD67 gene (Tamamaki et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Difference in Binocularity and Ocular Dominance Plasticity between GABAergic and Excitatory Cortical Neurons

Kameyama¹,

Sohya²,

Ebina³

et al. 2010

J. Neurosci.

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Neuronal circuits in the cerebral cortex consist mainly of glutamatergic/excitatory and GABAergic/inhibitory neurons. In the visual cortex, the binocular responsiveness of neurons is modified by monocular visual deprivation during the critical period of postnatal development. Although GABAergic neurons are considered to play a key role in the expression of the critical period, it is not known whether their binocular responsiveness and ocular dominance plasticity are different from those of excitatory neurons. Recently, the end of the critical period was found to be not strict so that cortical neurons in the adult still have some ocular dominance plasticity. It is not known, however, which type of neurons or both maintain such plasticity in adulthood. To address these issues, we applied in vivo two-photon functional Ca 2ϩ imaging to transgenic mice whose GABAergic neurons express a yellow fluorescent protein called Venus. We found that GABAergic neurons are more binocular than excitatory neurons in the normal visual cortex, and both types of neurons show the same degree of modifiability to monocular visual deprivation during the critical period, but the modifiability of GABAergic neurons is stronger than that of excitatory neurons after the end of the critical period.

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Section: Binocularity Of Gabaergic Neuronscontrasting

confidence: 55%

Section: Introductionmentioning

confidence: 99%

Difference in Binocularity and Ocular Dominance Plasticity between GABAergic and Excitatory Cortical Neurons

Kameyama¹,

Sohya²,

Ebina³

et al. 2010

J. Neurosci.

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“…Figure 3A shows examples of PSP and AP responses of pyramidal neurons of the various laminae, averaged over 30 stimulus presentations. For each neuron, I computed an ocular dominance index (ODI), defined as (C Ϫ I)/(C ϩ I), where C and I are the amplitudes of visual responses to independent contralateral and ipsilateral eye stimulation, respectively (Rittenhouse et al, 1999;Pizzorusso et al, 2002;Mrsic-Flogel et al, 2007;Gandhi et al, 2008). This index varies from Ϫ1 to ϩ1 depending on whether cells are dominated by the ipsilateral or contralateral eye, respectively, whereas the ODI is 0 for perfectly binocular neurons.…”

Section: Binocularity Of Synaptic Inputs Is Not Uniform: Psp Responsementioning

confidence: 99%

“…However, even when the recording positions were reconstructed (Shatz and Stryker, 1978;Gordon and Stryker, 1996;Issa et al, 1999), the identity of recorded neurons remained uncertain. This is important because plasticity is cell-type specific even within a layer (Gandhi et al, 2008;Mainardi et al, 2009;Yazaki-Sugiyama et al, 2009). In addition, extracellular recordings are biased toward highly spiking cells, and firing rates depend on the laminar and cellular identity in rodent V1 (Niell and Stryker, 2008;Medini, 2011).…”

Section: Introductionmentioning

confidence: 99%

Layer- and Cell-Type-Specific Subthreshold and Suprathreshold Effects of Long-Term Monocular Deprivation in Rat Visual Cortex

Medini¹

2011

J. Neurosci.

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Connectivity and dendritic properties are determinants of plasticity that are layer and cell-type specific in the neocortex. However, the impact of experience-dependent plasticity at the level of synaptic inputs and spike outputs remains unclear along vertical cortical microcircuits. Here I compared subthreshold and suprathreshold sensitivity to prolonged monocular deprivation (MD) in rat binocular visual cortex in layer 4 and layer 2/3 pyramids (4Ps and 2/3Ps) and in thick-tufted and nontufted layer 5 pyramids (5TPs and 5NPs), which innervate different extracortical targets. In normal rats, 5TPs and 2/3Ps are the most binocular in terms of synaptic inputs, and 5NPs are the least. Spike responses of all 5TPs were highly binocular, whereas those of 2/3Ps were dominated by either the contralateral or ipsilateral eye. MD dramatically shifted the ocular preference of 2/3Ps and 4Ps, mostly by depressing deprived-eye inputs. Plasticity was profoundly different in layer 5. The subthreshold ocular preference shift was sevenfold smaller in 5TPs because of smaller depression of deprived inputs combined with a generalized loss of responsiveness, and was undetectable in 5NPs. Despite their modest ocular dominance change, spike responses of 5TPs consistently lost their typically high binocularity during MD. The comparison of MD effects on 2/3Ps and 5TPs, the main affected output cells of vertical microcircuits, indicated that subthreshold plasticity is not uniquely determined by the initial degree of input binocularity. The data raise the question of whether 5TPs are driven solely by 2/3Ps during MD. The different suprathreshold plasticity of the two cell populations could underlie distinct functional deficits in amblyopia.

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“…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 (14). Previous work attempted to track ODP in individual cortical neurons over time (15), but did not address the relative time course and nature of plastic changes in excitatory vs. inhibitory circuits during ODP (10,(16)(17)(18). The role for ongoing network activity in sleep (vs. waking experience) in these processes is also unknown.…”

mentioning

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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Delayed plasticity of inhibitory neurons in developing visual cortex

Cited by 105 publications

References 40 publications

Difference in Binocularity and Ocular Dominance Plasticity between GABAergic and Excitatory Cortical Neurons

Difference in Binocularity and Ocular Dominance Plasticity between GABAergic and Excitatory Cortical Neurons

Layer- and Cell-Type-Specific Subthreshold and Suprathreshold Effects of Long-Term Monocular Deprivation in Rat Visual Cortex

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

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