Distinct Roles for Spontaneous and Visual Activity in Remodeling of the Retinogeniculate Synapse

Hooks, Bryan M.; Chen, Chinfei

doi:10.1016/j.neuron.2006.07.007

Cited by 281 publications

(351 citation statements)

References 55 publications

(67 reference statements)

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“…To minimize light exposure before the animals were killed, experimental dark-reared animals were transferred to the lab in an opaque box. Our data for chronic DR and half the data for late DR are drawn from our previous study (Hooks and Chen, 2006).…”

Section: Methodsmentioning

confidence: 99%

“…In contrast, subcortical regions, including thalamus, superior colliculus, and retina, were thought to develop earlier and be less sensitive to sensory experience. Recent studies, however, show that experience influences circuit development and maintenance in the retina (Tian and Copenhagen, 2003), superior colliculus (Lu and Constantine-Paton, 2004;Carrasco et al, 2005), and thalamus (Hooks and Chen, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…Specifically, excess retinal afferents to relay cells prune and remaining afferents strengthen. Spontaneous retinal activity, not vision, drives these functional changes (Hooks and Chen, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…Specifically, dark rearing mice from postnatal day 20 (p20), called late dark rearing (late DR), results in recruitment of additional retinal inputs and weakening of existing inputs innervating thalamic relay neurons (Hooks and Chen, 2006). Thus, changes in visual experience alter circuit connectivity.…”

Section: Introductionmentioning

confidence: 99%

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Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse

Hooks

Chen²

2008

J. Neurosci.

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In the mammalian visual system, sensory experience is widely thought to sculpt cortical circuits during a precise critical period. In contrast, subcortical regions, such as the thalamus, were thought to develop at earlier ages in a vision-independent manner. Recent studies at the retinogeniculate synapse, however, have demonstrated an influence of vision on the formation of synaptic circuits in the thalamus. In mice, dark rearing from birth does not alter normal developmental maturation of the connection between retina and thalamus. However, deprivation 20 d after birth [postnatal day 20 (p20)] resulted in dramatic weakening of synaptic strength and an increase in the number of retinal inputs that innervate a thalamic relay neuron. Here, by quantifying changes in synaptic strength and connectivity in response to different time windows of deprivation, we find that several days of vision after eye opening is necessary for triggering experience-dependent plasticity. Shorter periods of visual experience do not permit similar experience-dependent synaptic reorganization. Furthermore, changes in connectivity are rapidly reversible simply by restoring normal vision. However, similar plasticity did not occur when shifting the onset of deprivation to p25. Although synapses still weakened, recruitment of additional retinal inputs no longer occurred. Therefore, synaptic circuits in the visual thalamus are unexpectedly malleable during a late developmental period, after the time when normal synapse elimination and pruning has occurred. This thalamic sensitive period overlaps temporally with experience-dependent changes in the cortex, suggesting that subcortical plasticity may influence cortical responses to sensory experience.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse

Hooks

Chen²

2008

J. Neurosci.

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“…Specifically, can altered voltage-dependent activity in central projection neurons perturb the glomerular homogeneity or destabilize the synaptic connections that formulate the sensory map? In the retina, block of voltage-gated sodium channel activity results in pathfinding defects of axonal projections that overshoot their synaptic targets or else acts to retard synaptic strengthening (i.e., Hooks and Chen, 2006). We have examined mice with a gene-targeted deletion of the Kv1.3 ion channel (Kv1.3 −/− ) to understand how voltagegated activity may influence olfactory coding or organization.…”

mentioning

confidence: 99%

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Biju

Marks

Mast

et al. 2007

J of Comparative Neurology

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Olfactory sensory neurons (OSNs) expressing a specific odorant receptor (OR) gene send axonal projections to specific glomeruli, creating a stereotypic olfactory sensory map. Odorant receptor sequence, G-protein cAMP signaling, and axon guidance molecules have been shown to direct axons of OSNs toward central targets in the olfactory bulb (OB). Although the OR sequence may act as one determinant, our objective was to elucidate the extent by which voltage-dependent activity of postsynaptic projection neurons in the OB centrally influences peripheral development and target destination of OSNs. We bred OR-tagged transgenic mice to homozygosity with mice that had a gene-targeted deletion of the Shaker potassium ion channel (Kv1.3) to elucidate how activity modulates synaptic connections that formulate the sensory map. Here we report that the Kv1.3 ion channel, which is predominantly expressed in mitral cells and whose gene-targeted deletion causes a "super-smeller" phenotype, alters synaptic refinement of axonal projections from OSNs expressing P2, M72, and MOR28 ORs. Absence of Kv1.3 voltage-gated activity caused the formation of small, heterogeneous, and supernumerary glomeruli that failed to undergo neural pruning over development. These changes were accompanied by a significant decrease in the number of P2-, M72-, and MOR28-expressing OSNs, which contained an overexpression of OR protein and G-protein G olf in the cilia of the olfactory epithelium. These findings suggest that voltage-gated activity of projection neurons is essential to refine primary olfactory projections and that it regulates proper expression of the transduction machinery at the periphery. Indexing termsolfactory coding; axon targeting; olfaction; odorant receptor; Kv1.3The development of precise connectivity and maintenance of an olfactory sensory map is thought to rely upon guidance molecules that are recognized by receptors on olfactory sensory neurons (OSNs) or that are regulated by G-protein-mediated cAMP signals (Bozza et al., 2002;St John et al., 2002;Imai et al., 2006; Lattermann et al., 2007;Sweeney et al., 2007). OSNs expressing a given olfactory receptor are primarily randomly dispersed within one of four zones in the main olfactory epithelium (Ressler et al., 1993;Vassar et al., 1993;Mombaerts et al., 1996) but send their axonal projections to spatially conserved glomeruli within the olfactory bulb (Mombaerts, 1996;Wang et al., 1998;Tsuboi et al., 1999). Thus the olfactory bulb (OB) serves as a two- NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript dimensional map of receptor activation to provide the neural code to discriminate olfactory sensory information (Yu et al., 2004). Odorant quality is thus encoded by a specific combination of activated glomeruli (Mori et al., 1999;Strotmann et al., 2000), and the formation of glomeruli depends on contextual sorting of axons expressing like OR proteins (Belluscio et al., 2002;Mombaerts, 2006).If contextual cues from adjacent homotypic interactions initiate...

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Identifying roles for neurotransmission in circuit assembly: Insights gained from multiple model systems and experimental approaches

Bleckert

Wong

2010

BioEssays

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In the adult nervous system, chemical neurotransmission between neurons is essential for information processing. However, neurotransmission is also important for patterning circuits during development, but its precise roles have yet to be identified, and some remain highly debated. Here, we highlight viewpoints that have come to be widely accepted or still challenged. We discuss how distinct techniques and model systems employed to probe the developmental role of neurotransmission may reconcile disparate ideas. We underscore how the effects of perturbing neurotransmission during development vary with model systems, the stage of development when transmission is altered, the nature of the perturbation, and how connectivity is assessed. Based on findings in circuits with connectivity arranged in layers, we raise the possibility that there exist constraints in neuronal network design that limit the role of neurotransmission. We propose that activity-dependent mechanisms are effective in refining connectivity patterns only when inputs from different cells are close enough spatially to influence each other’s outcome.

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Distinct Roles for Spontaneous and Visual Activity in Remodeling of the Retinogeniculate Synapse

Cited by 281 publications

References 55 publications

Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse

Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Identifying roles for neurotransmission in circuit assembly: Insights gained from multiple model systems and experimental approaches

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