Specific Effects of Neurotransmitter Antagonists on Ganglion Cells in Rabbit Retina

Wyatt, Harry J.; Day, Nigel W.

doi:10.1126/science.1857

Cited by 158 publications

(83 citation statements)

References 12 publications

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“…The relative importance of inhibition in mediating a cell's directional selectivity has been confirmed in many different structures and animals using the same Barlow and Levick paradigm (Ganz and Felder, 1984;Michael, 1965). The role of inhibition also received independent support from rcperimenr, where inhibitory synaptic transmission v.as disrupted pharmacologically with a consequent abolition of directional selectivity (Wyatt andDaw. 1976: Sitlito, 1977).…”

Section: Early Modelsmentioning

confidence: 99%

Biological image motion processing: A review

1985

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Section: Early Modelsmentioning

confidence: 99%

Biological image motion processing: A review

1985

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“…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.…”

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confidence: 96%

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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“…Subsequent studies showed that GABAergic antagonists abolish direction selectivity, suggesting that asymmetric inhibition resulting from null direction stimulus movement plays a crucial role (Barlow and Levick, 1965;Wyatt and Daw, 1976;Caldwell et al, 1978;Ariel and Daw, 1982;Kittila and Massey, 1995). Starburst amacrine cells, interneurons that release both acetylcholine and GABA, synapse onto DS cells and thus have been a favorite candidate for the source of GABAergic inhibition responsible for direction selectivity (Vaney et al, 1989;Famiglietti, 1991Famiglietti, , 1992.…”

Section: Introductionmentioning

confidence: 99%

A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

Ozaita¹,

Petit-Jacques²,

Völgyi³

et al. 2004

J. Neurosci.

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Direction-selective retinal ganglion cells show an increased activity evoked by light stimuli moving in the preferred direction. This selectivity is governed by direction-selective inhibition from starburst amacrine cells occurring during stimulus movement in the opposite or null direction. To understand the intrinsic membrane properties of starburst cells responsible for direction-selective GABA release, we performed whole-cell recordings from starburst cells in mouse retina. Voltage-clamp recordings revealed prominent voltagedependent K ϩ currents. The currents were mostly blocked by 1 mM TEA, activated rapidly at voltages more positive than Ϫ20 mV, and deactivated quickly, properties reminiscent of the currents carried by the Kv3 subfamily of K ϩ channels. Immunoblots confirmed the presence of Kv3.1 and Kv3.2 proteins in retina and immunohistochemistry revealed their expression in starburst cell somata and dendrites. The Kv3-like current in starburst cells was absent in Kv3.1-Kv3.2 knock-out mice. Current-clamp recordings showed that the fast activation of the Kv3 channels provides a voltage-dependent shunt that limits depolarization of the soma to potentials more positive than Ϫ20 mV. This provides a mechanism likely to contribute to the electrical isolation of individual starburst cell dendrites, a property thought essential for direction selectivity. This function of Kv3 channels differs from that in other neurons where they facilitate highfrequency repetitive firing. Moreover, we found a gradient in the intensity of Kv3.1b immunolabeling favoring proximal regions of starburst cells. We hypothesize that this Kv3 channel gradient contributes to the preference for centrifugal signal flow in dendrites underlying direction-selective GABA release from starburst amacrine cells

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Specific Effects of Neurotransmitter Antagonists on Ganglion Cells in Rabbit Retina

Cited by 158 publications

References 12 publications

Biological image motion processing: A review

Biological image motion processing: A review

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

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