A Key Role of Starburst Amacrine Cells in Originating Retinal Directional Selectivity and Optokinetic Eye Movement

Yoshida, Kazumichi; Watanabe, Dai; Ishikane, Hiroshi; Tachibana, Makoto; Pastan, Ira; Nakanishi, Shigetada

doi:10.1016/s0896-6273(01)00316-6

Cited by 330 publications

(307 citation statements)

References 31 publications

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“…Second, AChR KOs analyzed to date lack only some receptors, leaving other pathways for cholinergic transmission intact (Bansal et al, 2000;Rossi et al, 2001). Third, attempts to ablate retinal cholinergic neurons (i.e., starburst amacrine cells) were unable to completely eliminate these cells before synapse formation in the inner retina Reese et al, 2001;Yoshida et al, 2001;Huberman et al, 2003). Here, we used an alternate method that circumvents these limitations.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

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

et al. 2005

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“…These amacrine cells contain both acetylcholine and GABA and thus could contribute to both the excitatory and inhibitory mechanisms (Vaney et al, 1989;Borg-Graham and Grzywacz, 1992;Grzywacz et al, 1997). The role of starburst cells within the direction-selective circuit is controversial, however, with one report claiming that they are critical (Yoshida et al, 2001) and another claiming that they are not essential (He and Masland, 1997). Available evidence indicates that the two populations of starburst cells are structurally and functionally equivalent (except for the sign of their responses) (Bloomfield, 1992), and therefore they may underlie the presynaptic mechanisms that are common in the on-and off-responses.…”

Section: Implications For Synaptic Circuitrymentioning

confidence: 99%

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

2002

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The synaptic conductance of the On-Off direction-selective ganglion cells was measured during visual stimulation to determine whether the direction selectivity is a property of the circuitry presynaptic to the ganglion cells or is generated by postsynaptic interaction of excitatory and inhibitory inputs. Three synaptic asymmetries were identified that contribute to the generation of direction-selective responses: (1) a presynaptic mechanism producing stronger excitation in the preferred direction, (2) a presynaptic mechanism producing stronger inhibition in the opposite direction, and (3) postsynaptic interaction of excitation with spatially offset inhibition. Although the on-and off-responses showed the same directional tuning, the off-response was generated by all three mechanisms, whereas the on-response was generated primarily by the two presynaptic mechanisms. The results indicate that, within a single neuron, different strategies are used within distinct dendritic arbors to accomplish the same neural computation.Key words: direction selectivity; ganglion cells; synaptic conductance; inhibition; excitation; dendritic integration; on-and off-pathways; rabbit retinaThe direction-selective ganglion cells (DSGCs) in the rabbit retina are a model system for investigating neural computation (Vaney et al., 2001). These cells respond strongly to an image moving in a preferred direction but only weakly to an image moving in the opposite "null" direction. The foundation for understanding the cellular mechanisms of direction selectivity in vertebrates was laid by Barlow and Levick (1965), whose extracellular recordings from DSGCs indicated that direction selectivity was mediated primarily by inhibition activated by nulldirection image motion. Strong support for the inhibitory model was provided by subsequent pharmacological experiments, which showed that GABA A -receptor antagonists abolish direction selectivity (Wyatt and Daw, 1976;Ariel and Daw, 1982;Kittila and Massey, 1997). However, these extracellular recording experiments provided no information about whether the inhibition acted directly on the DSGC or presynaptically on the excitatory interneurons.Torre and Poggio (1978) proposed a postsynaptic model in which DSGCs receive an inhibitory input that is spatially offset relative to the excitatory input; moreover, the inhibition is nondirectional, being activated equally well by image motion in the preferred and null directions. During null-direction motion, the spatial offset means that delayed inhibitory synapses at locations ahead of the stimulus are activated and veto the excitation as the stimulus sweeps across the receptive field. For preferreddirection motion, the inhibition trails behind the stimulus and thus arrives too late to veto the excitation. For this model to work, the inhibition must act locally within the dendritic arbor of the DSGC. This occurs when the inhibitory reversal potential is at, or close to, the resting potential of the cell, and therefore the inhibitory input does not polarize the c...

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“…There is evidence that the axon-bearing amacrine cells electrically coupled to ganglion cells contain cholecystokinin (Jacoby et al, 1996). It might therefore be possible to use immunotoxin-mediated cell-targeting techniques, such as have been used to eliminate cholinergic amacrine cells (Yoshida et al, 2001), or cell ablation methods tied to the expression of a particular peptide (Nirenberg & Meister, 1997), to directly investigate the contribution of axon-bearing amacrine cells to the generation of HFOPs. Knock-outs deficient in specific connexins have been used to assess the role of gap junctions in normal light responses (Guldenagel et al, 2001) and in the generation of gamma oscillations (Hormuzdi et al, 2001), raising the possibility that selective ablation of gap junctions between amacrine cells and ganglion cells may soon be experimentally feasible.…”

Section: Predictions Of the Modelmentioning

confidence: 99%

A model of high-frequency oscillatory potentials in retinal ganglion cells

et al. 2003

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High-frequency oscillatory potentials (HFOPs) have been recorded from ganglion cells in cat, rabbit, frog, and mudpuppy retina and in electroretinograms (ERGs) from humans and other primates. However, the origin of HFOPs is unknown. Based on patterns of tracer coupling, we hypothesized that HFOPs could be generated, in part, by negative feedback from axon-bearing amacrine cells excited via electrical synapses with neighboring ganglion cells. Computer simulations were used to determine whether such axon-mediated feedback was consistent with the experimentally observed properties of HFOPs. (1) Periodic signals are typically absent from ganglion cell PSTHs, in part because the phases of retinal HFOPs vary randomly over time and are only weakly stimulus locked. In the retinal model, this phase variability resulted from the nonlinear properties of axon-mediated feedback in combination with synaptic noise. (2) HFOPs increase as a function of stimulus size up to several times the receptive-field center diameter. In the model, axon-mediated feedback pooled signals over a large retinal area, producing HFOPs that were similarly size dependent. (3) HFOPs are stimulus specific. In the model, gap junctions between neighboring neurons caused contiguous regions to become phase locked, but did not synchronize separate regions. Model-generated HFOPs were consistent with the receptive-field center dynamics and spatial organization of cat alpha cells. HFOPs did not depend qualitatively on the exact value of any model parameter or on the numerical precision of the integration method. We conclude that HFOPs could be mediated, in part, by circuitry consistent with known retinal anatomy.

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A Key Role of Starburst Amacrine Cells in Originating Retinal Directional Selectivity and Optokinetic Eye Movement

Cited by 330 publications

References 31 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

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

A model of high-frequency oscillatory potentials in retinal ganglion cells

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