Spontaneous Retinal Activity Mediates Development of Ocular Dominance Columns and Binocular Receptive Fields in V1

Huberman, Andrew D.; Speer, Colenso M.; Chapman, Barbara

doi:10.1016/j.neuron.2006.07.028

Cited by 118 publications

(99 citation statements)

References 43 publications

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“…In the present study, we investigated the impact of cholinergic input on the oscillatory activity of the visual cortex during the first postnatal week, which is a critical period for the fine-tuning of the geniculocortical connections (Cang et al, 2005;del Rio and Feller, 2006;Huberman et al, 2006). Using in vivo recordings from V1 of neonatal rats paired with short-term and long-term modification of the cholinergic input, we showed that (1) acute pharmacological blockade of the cortical mAChR or increase in the ACh level modulates both spontaneous and retina-triggered V1 spindle bursts, (2) electrical stimulation of the BFn responsible for the cortical cholinergic input elicits V1 spindle bursts, and (3) irreversible immunotoxic lesion of the BFn dramatically diminishes the oscillatory spindle bursts activity of the V1 cortex.…”

Section: Discussionmentioning

confidence: 99%

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

Hanganu¹,

Staiger²,

Ben-Ari³

et al. 2007

J. Neurosci.

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Acetylcholine (ACh) is known to shape the adult neocortical activity related to behavioral states and processing of sensory information. However, the impact of cholinergic input on the neonatal neuronal activity remains widely unknown. Early during development, the principal activity pattern in the primary visual (V1) cortex is the intermittent self-organized spindle burst oscillation that can be driven by the retinal waves. Here, we assessed the relationship between this early activity pattern and the cholinergic drive by either blocking or augmenting the cholinergic input and investigating the resultant effects on the activity of the rat visual cortex during the first postnatal week in vivo. Blockade of the muscarinic receptors by intracerebroventricular, intracortical, or supracortical atropine application decreased the occurrence of V1 spindle bursts by 50%, both the retina-independent and the optic nerve-mediated spindle bursts being affected. In contrast, blockade of acetylcholine esterase with physostigmine augmented the occurrence, amplitude, and duration of V1 spindle bursts. Whereas direct stimulation of the cholinergic basal forebrain nuclei increased the occurrence probability of V1 spindle bursts, their chronic immunotoxic lesion using 192 IgG-saporin decreased the occurrence of neonatal V1 oscillatory activity by 87%. Thus, the cholinergic input facilitates the neonatal V1 spindle bursts and may prime the developing cortex to operate specifically on relevant early (retinal waves) and later (visual input) stimuli.

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Section: Discussionmentioning

confidence: 99%

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

Hanganu¹,

Staiger²,

Ben-Ari³

et al. 2007

J. Neurosci.

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“…The visual cortex in mice has several well-defined periods under which various developmental processes take place. The period from birth to postnatal day 14 (P14) is characterized by the development of retinotopy and the creation of binocular responses (4,5) whereas the period of P21-P35 is known as the "critical period" for ocular dominance plasticity where binocularity and binocular matching develop, with its peak at P26 (4,6). Although great progress has been made in elucidating changes in connectivity and function during the postnatal maturation of the mouse visual cortex, the transcriptional programs enabling these developmental events are still unknown.…”

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confidence: 99%

Transcriptomics of critical period of visual cortical plasticity in mice

Benoit

Ayoub

Rakić

2015

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

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In contrast to the prenatal development of the cerebral cortex, when cell production, migration, and layer formation dominate, development after birth involves more subtle processes, such as activity-dependent plasticity that includes refinement of synaptic connectivity by its stabilization and elimination. In the present study, we use RNA-seq with high spatial resolution to examine differential gene expression across layers 2/3, 4, 5, and 6 of the mouse visual cortex before the onset of the critical period of plasticity [postnatal day 5 (P5)], at its peak (P26), and at the mature stage (P180) and compare it with the prefrontal association area. We find that, although genes involved in early developmental events such as cell division, neuronal migration, and axon guidance are still prominent at P5, their expression largely terminates by P26, when synaptic plasticity and associated signaling pathways become enriched. Unexpectedly, the gene expression profile was similar in both areas at this age, suggesting that activity-dependent plasticity between visual and association cortices are subject to the same genetic constraints. Although gene expression changes follow similar paths until P26, we have identified 30 regionally enriched genes that are prominent during the critical period. At P180, we identified several hundred differentially expressed gene isoforms despite subsiding levels of gene expression differences. This result indicates that, once genetic developmental programs cease, the remaining morphogenetic processes may depend on posttranslational events.

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“…The role of synaptic transmission in the refinement of central synapses seems more complex. Although manipulations of presynaptic activity disrupted the refinement of connections in the visual pathway (15)(16)(17), some of the effects were independent of synaptic transmission (18,19).…”

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Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses

Zhang

Peterson

Liu

2012

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

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Neurons in the brains of newborns are usually connected with many other neurons through weak synapses. This early pattern of connectivity is refined through pruning of many immature connections and strengthening of the remaining ones. NMDA receptors (NMDARs) are essential for the development of excitatory synapses, but their role in synaptic refinement is controversial. Although chronic application of blockers or global knockdown of NMDARs disrupts developmental refinement in many parts of the brain, the ubiquitous presence of NMDARs makes it difficult to dissociate direct effects from indirect ones. We addressed this question in the thalamus by using genetic mosaic deletion of NMDARs. We demonstrate that pruning and strengthening of immature synapses are blocked in neurons without NMDARs, but occur normally in neighboring neurons with NMDARs. Our data support a model in which activation of NMDARs in postsynaptic neurons initiates synaptic refinement.D uring early development in vertebrates, neurons in many parts of the nervous system form weak synapses with a large number of target cells (1-7). This early pattern of connectivity is refined through two processes: synapse elimination that removes many initial connections and synapse maturation whereby the remaining connections are strengthened (8,9). This refinement of immature synapses is essential for the formation of neural circuits, and provides the basis for behavioral development. Many studies, in particular those conducted at the neuromuscular junction, in the cerebellum and visual pathways, have demonstrated that activity plays a central role in synaptic refinement (10-12). However, the mechanisms of synaptic refinement remain incompletely understood. At the neuromuscular junction, silencing of synaptic transmission disrupted the refinement process (13,14). The role of synaptic transmission in the refinement of central synapses seems more complex. Although manipulations of presynaptic activity disrupted the refinement of connections in the visual pathway (15-17), some of the effects were independent of synaptic transmission (18,19).The vast majority of excitatory synapses in the brain use glutamate as neurotransmitter; synaptic transmission is usually mediated by AMPA receptors (AMPARs) and NMDA receptors (NMDARs) in postsynaptic neurons. NMDARs play an important role in the development of neural circuits. In the brains of neonates, glutamatergic synapses have few or no AMPARs, and synaptic transmission is primarily mediated by NMDARs (20-23). Activation of NMDARs by correlated activity is thought to be a key mechanism underlying synaptic refinement during development (24, 25). Consistent with this idea, chronic application of NMDAR antagonists or global knockdown of NMDARs disrupts developmental refinement of neuronal circuits in many parts of the brain (26-28). However, recent studies in the hippocampus have shown that single-cell deletion of NMDARs in newborn mice has no effect on the number or density of synaptic spines (29). These findings raised the...

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Spontaneous Retinal Activity Mediates Development of Ocular Dominance Columns and Binocular Receptive Fields in V1

Cited by 118 publications

References 43 publications

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

Transcriptomics of critical period of visual cortical plasticity in mice

Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses

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