Mechanisms Underlying Developmental Changes in the Firing Patterns of ON and OFF Retinal Ganglion Cells during Refinement of their Central Projections

Myhr, Karen L.; Lukasiewicz, Peter D.; Wong, Rachel

doi:10.1523/jneurosci.21-21-08664.2001

Cited by 52 publications

(47 citation statements)

References 35 publications

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“…There is little information about the electrophysiological properties of identified ON and OFF cells in the functionally intact retina. Differences in the firing thresholds of these cells in the developing retina have been reported (Myhr et al, 2001), but no systematic studies have been done on intact adult RGCs (but see O'Brien et al, 2002;Zaghloul et al, 2003). Our results demonstrate that intrinsic differences last into adulthood and represent a fundamental feature of mature retina.…”

Section: Different Intrinsic Properties For On and Off Rgcsmentioning

confidence: 50%

Different Mechanisms Generate Maintained Activity in ON and OFF Retinal Ganglion Cells

Margolis¹,

Detwiler²

2007

J. Neurosci.

196

327

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Neuronal discharge is driven by either synaptic input or cell-autonomous intrinsic pacemaker activity. It is commonly assumed that the resting spike activity of retinal ganglion cells (RGCs), the output cells of the retina, is driven synaptically, because retinal photoreceptors and second-order cells tonically release neurotransmitter. Here we show that ON and OFF RGCs generate maintained activity through different mechanisms: ON cells depend on tonic excitatory input to drive resting activity, whereas OFF cells continue to fire in the absence of synaptic input. In addition to spontaneous activity, OFF cells exhibit other properties of pacemaker neurons, including subthreshold oscillations, burst firing, and rebound excitation. Thus, variable weighting of synaptic mechanisms and intrinsic properties underlies differences in the generation of maintained activity in these parallel retinal pathways.

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Section: Different Intrinsic Properties For On and Off Rgcsmentioning

confidence: 50%

Different Mechanisms Generate Maintained Activity in ON and OFF Retinal Ganglion Cells

Margolis¹,

Detwiler²

2007

J. Neurosci.

196

327

View full text Add to dashboard Cite

show abstract

“…Changes to the network during the period of synchronized activity in the retina, cortex, or spinal cord include differentiation of novel cell types, formation and elimination of synapses, and maturation of distinct neurotransmitter pathways. The intrinsic biophysical properties of neurons also change with maturation, reducing excitability in some cells and increasing it in others (Zhou and Fain, 1996;Wang et al, 1997;Rothe et al, 1999;Myhr et al, 2001). Homeostatic mechanisms must exist to ensure maintenance of patterned spontaneous activity during development, yet little is known about such mechanisms in the CNS.…”

Section: Discussionmentioning

confidence: 99%

“…A third possibility is that GABAergic and glycinergic drive, which are depolarizing in the neonatal retina and modulate waves, could have increased to enable wave propagation in the KO region (Fischer et al, 1998;Wong et al, 1998Wong et al, , 2000Myhr et al, 2001;Zhou, 2001). Such GABAergic and glycinergic synaptic upregulation is seen in the developing spinal cord in response to cholinergic and glutamatergic blockade .…”

Section: Mechanisms Underlying Ko and Wt Waves Are Distinctmentioning

confidence: 99%

Disruption and Recovery of Patterned Retinal Activity in the Absence of Acetylcholine

et al. 2005

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Many developing neural circuits generate synchronized bursting activity among neighboring neurons, a pattern thought to be important for sculpting precise neural connectivity. Network output remains relatively constant as the cellular and synaptic components of these immature circuits change during development, suggesting the presence of homeostatic mechanisms. In the retina, spontaneous waves of activity are present even before chemical synapse formation, needing gap junctions to propagate. However, as synaptogenesis proceeds, retinal waves become dependent on cholinergic neurotransmission, no longer requiring gap junctions. Later still in development, waves are driven by glutamatergic rather than cholinergic synapses. Here, we asked how retinal activity evolves in the absence of cholinergic transmission by using a conditional mutant in which the gene encoding choline acetyltransferase (ChAT), the sole synthetic enzyme for acetylcholine (ACh), was deleted from large retinal regions. ChAT-negative regions lacked retinal waves for the first few days after birth, but by postnatal day 5 (P5), ACh-independent waves propagated across these regions. Pharmacological analysis of the waves in ChAT knock-out regions revealed a requirement for gap junctions but not glutamate, suggesting that patterned activity may have emerged via restoration of previous gap-junctional networks. Similarly, in P5 wild-type retinas, spontaneous activity recovered after a few hours in nicotinic receptor antagonists, often as local patches of coactive cells but not waves. The rapid recovery of rhythmic spontaneous activity in the presence of cholinergic antagonists and the eventual emergence of waves in ChAT knock-out regions suggest that homeostatic mechanisms regulate retinal output during development.

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“…For example, the onset of glutamate waves leads to ON and OFF RGCs acquiring distinct spontaneous firing properties (Myhr et al, 2001). These distinct firing properties are thought to cause the segregation of ON and OFF laminas in the ferret LGN (Lee et al, 2002).…”

Section: Competing Instructive Signals May Limit Topographic Refinementmentioning

confidence: 99%

Developmental Homeostasis of Mouse Retinocollicular Synapses

Chandrasekaran¹,

Shah²,

Crair³

2007

J. Neurosci.

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) that lack correlated waves, retinocollicular map refinement is impaired. In vivo recordings reveal that neurons in the superior colliculus of ␤2 Ϫ/Ϫ mice have large receptive fields and low peak visual responses, resulting in a conservation of total integrated response. We find that this "response homeostasis" is maintained on a cell-bycell basis, and argue that it does not depend on regulation from the visual cortex during adulthood. Instead, in vitro recordings show that homeostasis arises from the conservation of total synaptic input from the retina, and that it is maintained via different mechanisms over development. In the absence of correlated retinal waves, ␤2Ϫ/Ϫ neurons sample a larger number of weaker retinal inputs relative to controls after the first postnatal week. Once retinal waves are restored, developmental learning rules and homeostasis drive refinement so that fewer, stronger synapses are retained, as in wild-type mice, but from a larger retinal area. Homeostasis in neurons has been shown previously to regulate the gain of synaptic transmission in response to perturbations of activity. Our results suggest that during the development of sensory maps, a unique consequence of homeostatic mechanisms is the precise shaping of neuronal receptive fields in conjunction with activity-dependent competition.

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Mechanisms Underlying Developmental Changes in the Firing Patterns of ON and OFF Retinal Ganglion Cells during Refinement of their Central Projections

Cited by 52 publications

References 35 publications

Different Mechanisms Generate Maintained Activity in ON and OFF Retinal Ganglion Cells

Different Mechanisms Generate Maintained Activity in ON and OFF Retinal Ganglion Cells

Disruption and Recovery of Patterned Retinal Activity in the Absence of Acetylcholine

Developmental Homeostasis of Mouse Retinocollicular Synapses

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