Stage‐dependent dynamics and modulation of spontaneous waves in the developing rabbit retina

Syed, Muhammad Ali; Lee, Seung‐Hoon; Zheng, Jijian; Zhou, Zhimin

doi:10.1113/jphysiol.2004.066597

Cited by 115 publications

(217 citation statements)

References 43 publications

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“…However, unlike wt waves at this age, waves in the ChAT KO region depend on gap junctions. Indeed, the ChAT KO waves share spatiotemporal characteristics with gap-junctionally mediated waves of the wt retina before synaptogenesis (Catsicas et al, 1998;Syed et al, 2004b). During the period when cholinergic transmission underlies wave propagation, L-type voltage-gated Ca 2ϩ channel agonists increase cellular coupling and induce waves propagated via gap junctions, even when cholinergic transmission is blocked (Singer et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

“…Pharmacological studies show that the circuitry underlying synchronized activity alters systematically with development. Before synaptogenesis, gap junctions are responsible (Peinado et al, 1993;Catsicas et al, 1998;Wong et al, 1998;Roerig and Feller, 2000;Syed et al, 2004b), but after synapse formation, chemical neurotransmission drives correlated activity (Leinekugel et al, 1997;O'Donovan et al, 1998;O'Donovan, 1999;Bansal et al, 2000;Wong et al, 2000;Zhou and Zhao, 2000;Syed et al, 2004b). In the spinal cord and retina, synchronized activity is first dependent on cholinergic transmission and thereafter on glutamatergic transmission.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2005

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“…Only one class of cells in the retina, the starburst amacrine cell, releases acetylcholine (ACh) (Zhou, 2001). Starburst amacrine cells undergo spontaneous depolarizations (Zheng et al, 2006) and release both ACh and GABA onto neighboring starburst amacrine cells and onto RGCs during retinal waves (Syed et al, 2004b;Zheng et al, 2006). To determine the effect of GABA A agonists on the cells presynaptic to RGCs, we recorded from SACs.…”

Section: Endogenous Tonic Activation Of Gaba a Receptors On Sacs But mentioning

confidence: 99%

“…Endogenous activation of GABA A receptors alters correlation structure of spontaneous firing patterns GABA A receptor antagonists do not block retinal waves, nor do they alter the global spatial and temporal properties of waves as assayed with calcium imaging [but see Fischer et al (1998), Stellwagen et al (1999, Catsicas and Mobbs (2001), Sernagor et al (2003), and Syed et al (2004b)]. To determine the effects of endogenous GABA signaling on the detailed spontaneous firing properties of RGCs, we used a multielectrode array, which allowed us to record extracellularly from many RGCs simultaneously (Meister et al, 1991;Wong et al, 1993;McLaughlin et al, 2003).…”

Section: Endogenous Tonic Activation Of Gaba a Receptors On Sacs But mentioning

confidence: 99%

“…In this study, we focus on retinal waves that occur between birth [postnatal day 0 (P0)] and P7 in mice and rats, which propagate through a network of interconnected cholinergic interneurons, the starburst amacrine cells (SACs) (Zheng et al, 2006). At these ages, retinal ganglion cells (RGCs) (Feller et al, 1996) and starburst amacrine cells (Syed et al, 2004b) receive barrages of GABAergic inputs, and activation of GABA A receptors is depolarizing in RGCs (Fischer et al, 1998;Stellwagen et al, 1999;Johnson et al, 2003;Zhang et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Wang

Blankenship²,

Anishchenko³

et al. 2007

J. Neurosci.

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Ambient GABA modulates firing patterns in adult neural circuits by tonically activating extrasynaptic GABA A receptors. Here, we demonstrate that during a developmental period when activation of GABA A receptors causes membrane depolarization, tonic activation of GABA A receptors blocks all spontaneous activity recorded in retinal ganglion cells (RGCs) and starburst amacrine cells (SACs). Bath application of the GABA A receptor agonist muscimol blocked spontaneous correlated increases in intracellular calcium concentration and compound postsynaptic currents in RGCs associated with retinal waves. In addition, GABA A receptor agonists activated a tonic current in RGCs that significantly reduced their excitability. Using a transgenic mouse in which green fluorescent protein is expressed under the metabotropic glutamate receptor subtype 2 promoter to target recordings from SACs, we found that GABA A receptor agonists blocked compound postsynaptic currents and also activated a tonic current. GABA A receptor antagonists reduced the holding current in SACs but not RGCs, indicating that ambient levels of GABA tonically activate GABA A receptors in SACs. GABA A receptor antagonists did not block retinal waves but did alter the frequency and correlation structure of spontaneous RGC firing. Interestingly, the drug aminophylline, a general adenosine receptor antagonist used to block retinal waves, induced a tonic GABA A receptor antagonist-sensitive current in outside-out patches excised from RGCs, indicating that aminophylline exerts its action on retinal waves by direct activation of GABA A receptors. These findings have implications for how various neuroactive drugs and neurohormones known to modulate extrasynaptic GABA A receptors may influence spontaneous firing patterns that are critical for the establishment of adult neural circuits.

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Expression and function of the neuronal gap junction protein connexin 36 in developing mammalian retina

Hansen

Torborg

Elstrott

et al. 2005

J of Comparative Neurology

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With the advent of transgenic mice, much has been learned about the expression and function of gap junctions. Previously, we reported that retinal ganglion cells in mice lacking the neuronal gap junction protein connexin 36 (Cx36) have nearly normal firing patterns at postnatal day 4 (P4) but many more asynchronous action potentials than wild-type mice at P10 (Torborg et al. [2005] Nat. Neurosci. 8:72-78). With the goal of understanding the origin of this increased activity in Cx36-/- mice, we used a transgenic mouse (Deans et al. [2001] Neuron 31:477-485) to characterize the developmental expression of a Cx36 reporter in the retina. We found that Cx36 was first detected weakly at P2 and gradually increased in expression until it reached an adult pattern at P14. Although the onset of expression varied by cell type, we identified Cx36 in the glycinergic AII amacrine cell, glutamatergic cone bipolar cell, and retinal ganglion cells (RGCs). In addition, we used calcium imaging and multielectrode array recording to characterize further the firing patterns in Cx36-/- mice. Both correlated and asynchronous action potentials in P10 Cx36-/- RGCs were significantly inhibited by bath application of an ionotropic glutamate receptor antagonist, indicating that the increase in activity was synaptically mediated. Hence, both the expression patterns and the physiology suggest an increasing role for Cx36-containing gap junctions in suppressing RGC firing between waves during postnatal retinal development.

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Stage‐dependent dynamics and modulation of spontaneous waves in the developing rabbit retina

Abstract: We report here a systematic investigation of the dynamics, regulation and distribution of spontaneous waves in the rabbit retina during the course of wave development prior to eye opening. Three major findings were obtained in this longitudinal study.

Cited by 115 publications

References 43 publications

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

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

GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Expression and function of the neuronal gap junction protein connexin 36 in developing mammalian retina

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Stage‐dependent dynamics and modulation of spontaneous waves in the developing rabbit retina

Abstract: We report here a systematic investigation of the dynamics, regulation and distribution of spontaneous waves in the rabbit retina during the course of wave development prior to eye opening. Three major findings were obtained in this longitudinal study.

Cited by 115 publications

References 43 publications

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

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

GABAAReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Expression and function of the neuronal gap junction protein connexin 36 in developing mammalian retina

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Product

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GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina