Shift of Intracellular Chloride Concentration in Ganglion and Amacrine Cells of Developing Mouse Retina

Zhang, Lingli; Pathak, Hemal R.; Coulter, Douglas A.; Freed, Michael; Vardi, Noga

doi:10.1152/jn.00578.2005

Cited by 68 publications

(95 citation statements)

References 66 publications

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“…1C and Fig. S1A), in agreement with previously reported data (22). This early depolarizing action of GABA is not prevented by addition of the alternate energy substrate pyruvate (Table S1), in contrast to recent observations in both neocortex (11) and hippocampus (26).…”

Section: Gaba Switch Occurs Normally In Nicotinic Acetylcholine Recepsupporting

confidence: 93%

“…Calcium imaging has been established as a preferred method forassaying depolarizing effects because imaging allows us to monitor depolarization in many neurons simultaneously without perturbing [Cl − ] i . Several previous studies in RGCs have confirmed this approach by demonstrating that an increase in intracellular calcium concentration in response to activation of GABA A receptors corresponds to an E GABA that is depolarized compared with the resting membrane potential as determined by perforated patch recordings (15,22,23).Retinal neurons loaded with Oregon Green BAPTA-1 (OGB-1) acetoxymethyl ester (AM) displayed an increase in intracellular calcium concentration ([Ca 2+ ] i ) in response to short applications of depolarizing, high K + -containing solution ( Fig. 1 A and B).…”

mentioning

confidence: 83%

“…Retinal ganglion cells (RGCs) undergo a switch in their response to GABA during the first two postnatal weeks of development (21)(22)(23). In vivo recordings in zebrafish demonstrate that the timing of the GABA switch is critical for the timing of the development of light responses (24) and therefore might be linked to the onset of visual experience.…”

mentioning

confidence: 99%

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Non–cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity

Barkis

Ford²,

Feller³

2010

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

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During development, the effect of activating GABA A receptors switches from depolarizing to hyperpolarizing. Several environmental factors have been implicated in the timing of this GABA switch, including neural activity, although these observations remain controversial. By using acutely isolated retinas from KO mice and pharmacological manipulations in retinal explants, we demonstrate that the timing of the GABA switch in retinal ganglion cells (RGCs) is unaffected by blockade of specific neurotransmitter receptors or global activity. In contrast to RGCs in the intact retina, purified RGCs remain depolarized by GABA, indicating that the GABA switch is not cell-autonomous. Indeed, purified RGCs cocultured with dissociated cells from the superior colliculus or cultured in media conditioned by superior collicular cells undergo a normal switch. Thus, a diffusible signal that acts independent of local circuit activity regulates the maturation of GABAergic inhibition in mouse RGCs.A lthough GABA is the principal inhibitory neurotransmitter in the mature CNS, it is a robust source of excitation during development that is important for many developmental processes (1-4). The transition from excitatory to inhibitory action of GABA has been observed in a number of neural circuits and in many vertebrate species (5, 6) and the primary mechanisms underlying the switch are fairly well understood (7-11; reviewed in refs. 12-14). However, whether the timing of the GABA switch is modulated by local circuit activity (8,(15)(16)(17)(18) or occurs independent of activity (19,20) and is therefore intrinsic to developmental program of the cell remains controversial.Retinal ganglion cells (RGCs) undergo a switch in their response to GABA during the first two postnatal weeks of development (21-23). In vivo recordings in zebrafish demonstrate that the timing of the GABA switch is critical for the timing of the development of light responses (24) and therefore might be linked to the onset of visual experience. Chronic blockade of GABA A receptors (GABA A Rs) in turtle retina prevents the normal maturation of spontaneous firing patterns termed retinal waves and the maturation of adult-like chloride gradients, implicating early GABA signaling in the normal maturation of inhibitory circuits in retina (15). Based on these results, it has been proposed that the maturation of GABAergic inhibition is influenced by local network activity and is critical for the cessation of retinal waves (25).Here we explore factors that influence the timing of the GABA switch in mouse RGCs. By using three different preparations, we test whether the timing of the GABA switch is regulated by (i) local circuit activity in the retina, (ii) an intrinsic developmental program, or (iii) a diffusible, non-cell autonomous factor that operates independent of retinal activity. Results GABA Switch Occurs Normally in Nicotinic Acetylcholine Receptor-KORetinas. The timing of the GABA switch in retinal neurons in the ganglion cell layer (GCL) was determined by calcium imagi...

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Section: Gaba Switch Occurs Normally In Nicotinic Acetylcholine Recepsupporting

confidence: 93%

mentioning

confidence: 83%

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Non–cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity

Barkis

Ford²,

Feller³

2010

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

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“…KCC2 labeling was present in the OPL and INL, but failed to colocalize with SV2 in photoreceptor terminals; instead, the labeling was present in the post-synaptic sites of photoreceptor terminals and the INL. The absence of KCC2 in the photoreceptor terminals is similar to previous results in rat and primate retinas (Vu et al, 2000;Vardi et al, 2000), but not ferret retinas in which KCC2 is detected in photoreceptors (Zhang et al, 2006a(Zhang et al, , 2006b). …”

Section: Nkcc1 In Photoreceptor Terminals In Adult Mouse Retinassupporting

confidence: 90%

“…These results suggest that accumulating intracellular Cl − might have occurred when photoreceptor synapses were formed. However, we do not know whether KCC2 is transiently expressed in photoreceptors during development, as suggested in ferret retinas (Zhang et al, 2006a(Zhang et al, , 2006b). …”

Section: The Expression Of Nkcc1 In the Distal Retinal Synaptic Develmentioning

confidence: 88%

Spatial and temporal distribution patterns of Na-K-2Cl cotransporter in adult and developing mouse retinas

McKERNAN

Shen

2008

Vis Neurosci

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The Na-K-2Cl cotransporter (NKCC) is a Cl − uptake transporter that is responsible for maintaining a Cl − equilibrium potential positive to the resting potential in neurons. If NKCC is active, GABA and glycine can depolarize neurons. In view of the abundance of GABAergic and glycinergic synapses in retina, we undertook a series of studies using immunocytochemical techniques to determine the distribution of NKCC in retinas of both developing and adult mice. We found NKCC antibody (T4) labeling present in retinas from wild-type mice, but not in NKCC1-deficient mice, suggesting that the NKCC1 subtype is a major Cl − uptake transporter in mouse retina. Strong labeling of NKCC1 was present in horizontal cells and rod-bipolar dendrites in adult mice. Interestingly, we also found that a diffuse labeling pattern was present in photoreceptor terminals. However, NKCC1 was barely detectable in the inner retina of adult mice. Using an antibody against K-Cl cotransporter 2 (KCC2), we found that KCC2, a transporter that extrudes Cl − , was primarily expressed in the inner retina. The expression of NKCC1 in developing mouse retinas was studied from postnatal day (P) 1 to P21, NKCC1 labeling first appeared in the dendrites of horizontal and rod-bipolar cells as early as P7, followed by photoreceptor terminals between P10-P14; with expression gradually increasing concomitantly with the growth of synaptic terminals and dendrites throughout retinal development. In the inner retina, NKCC1 labeling was initially observed in the inner plexiform layer at P1, but labeling diminished after P5. The developmental increase in NKCC expression only occurred in the outer retina. Our results suggest that the distal synapses and synaptogenesis in mouse retinas undergo a unique process with a high intracellular Cl − presence due to NKCC1 expression.

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M

2010

Handbook of Biological Dyes and Stains

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Shift of Intracellular Chloride Concentration in Ganglion and Amacrine Cells of Developing Mouse Retina

Cited by 68 publications

References 66 publications

Non–cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity

Non–cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity

Spatial and temporal distribution patterns of Na-K-2Cl cotransporter in adult and developing mouse retinas

M

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