Evidence for Activity-Dependent Cortical Wiring: Formation of Interhemispheric Connections in Neonatal Mouse Visual Cortex Requires Projection Neuron Activity

Mizuno, H.; Hirano, Tomoo; Tagawa, Yoshiaki

doi:10.1523/jneurosci.1215-07.2007

Cited by 173 publications

(284 citation statements)

References 84 publications

(107 reference statements)

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“…Consistent with previous tracing studies, the authors observed that callosal projections in the contralateral hemisphere were restricted to a region between areas 17 and 18 with a strong enrichment of axon terminals in layers 1-3 and 5 ( Fig. 1 A) [Mizuno et al (2007), their Fig. 1 (http://www.jneurosci.org/cgi/content/ full/27/25/6760/F1)].…”

supporting

confidence: 86%

“…The best characterized studies are of thalamocortical projections from the lateral geniculate nucleus to cortical layer 4, where cortical neurons are thought to go through an early phase of target selection dependent on molecular cues, followed by an activity-dependent mechanism, which then refines and maintains the connectivity (Katz and Crowley, 2002). In a recent The Journal of Neuroscience paper, Mizuno et al (2007) add another piece to the puzzle by showing that neuronal activity in callosal neurons is necessary for the initial laminar-specific elaboration of their axons.…”

mentioning

confidence: 99%

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Firing to Wire: A Role for Activity in Establishing Layer Specificity in the Cortex: Figure 1.

Chao¹,

Wang²

2007

J. Neurosci.

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supporting

confidence: 86%

mentioning

confidence: 99%

Firing to Wire: A Role for Activity in Establishing Layer Specificity in the Cortex: Figure 1.

Chao¹,

Wang²

2007

J. Neurosci.

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“…The synaptic source of the high synaptic binocularity of 2/3Ps and 5TPs could be the callosum. Indeed, callosal fibers branch mostly in layers 2/3 and 5 in rodent V1 (Jacobson and Trojanowski, 1974;Mizuno et al, 2007), and their inactivation reduces binoc- Figure 10. Differences in suprathreshold plasticity between 2/3Ps and 5TPs.…”

Section: Discussionmentioning

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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“…Previous studies using neuronal silencing with Kir2.1 have suggested that presynaptic activity plays a dominant role in axon branching (27,29,30). In particular, competitive interactions between a retinal ganglion cell and adjacent cells have been suggested to be crucial in retinotectal axon branching (27).…”

Section: Discussionmentioning

confidence: 99%

Role of pre- and postsynaptic activity in thalamocortical axon branching

Yamada

Uesaka

Hayano

et al. 2010

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

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Axonal branching is thought to be regulated not only by genetically defined programs but also by neural activity in the developing nervous system. Here we investigated the role of pre-and postsynaptic activity in axon branching in the thalamocortical (TC) projection using organotypic coculture preparations of the thalamus and cortex. Individual TC axons were labeled with enhanced yellow fluorescent protein by transfection into thalamic neurons. To manipulate firing activity, a vector encoding an inward rectifying potassium channel (Kir2.1) was introduced into either thalamic or cortical cells. Firing activity was monitored with multielectrode dishes during culturing. We found that axon branching was markedly suppressed in Kir2.1-overexpressing thalamic cells, in which neural activity was silenced. Similar suppression of TC axon branching was also found when cortical cell activity was reduced by expressing Kir2.1. These results indicate that both preand postsynaptic activity is required for TC axon branching during development.D uring development, axons navigate to their target regions and form elaborate branches when they make synaptic connections with multiple target cells. It has been demonstrated that axon guidance to the target region is regulated by attractive and repulsive molecular cues that are expressed in particular spatiotemporal patterns (1). Similar molecular mechanisms are thought to influence axon branching (2). In addition, neural activity such as firing and synaptic activity can also affect branch formation (3-5). An intriguing and unanswered problem is how neural activity regulates axonal branching.The thalamocortical (TC) projection in the mammalian cortex is a well-characterized system in which to investigate activity-dependent axon branching. In the developing sensory cortices, TC axons form elaborate terminal arbors, whose size and complexity are altered by neural activity. In the primary visual cortex of higher mammals such as cats, ferrets, and monkeys, TC axons serving left and right eyes are segregated into eye-specific stripes (6). This segregation is established during development (7), but is disrupted by blockade of retinal activity (8, 9). Regarding individual axon arbors, it is known that after monocular deprivation, TC axons serving the deprived and nondeprived eyes shrink and expand their arbors, respectively (10, 11). A recent study in which monocular deprivation was combined with silencing cortical activity has further suggested that correlations between pre-and postsynaptic activity play a dominant role in segregation of axon arbors (12). In accordance with this view, molecular machinery in pre-and postsynaptic sites has also been shown to affect arbor formation of TC axons in the somatosensory cortex (13-15). However, the relative role of pre-and postsynaptic activity in TC axon branching remains unclear.To address this issue, we investigated TC axon branching in cocultures of the thalamus and cortex by manipulating the firing activity of thalamic (presynaptic) and cortical (...

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Evidence for Activity-Dependent Cortical Wiring: Formation of Interhemispheric Connections in Neonatal Mouse Visual Cortex Requires Projection Neuron Activity

Cited by 173 publications

References 84 publications

Firing to Wire: A Role for Activity in Establishing Layer Specificity in the Cortex: Figure 1.

Firing to Wire: A Role for Activity in Establishing Layer Specificity in the Cortex: Figure 1.

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

Role of pre- and postsynaptic activity in thalamocortical axon branching

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