The shape and arrangement of the cholinergic neurons in the rabbit retina

Tauchi, Masaki; Masland, Richard H.

doi:10.1098/rspb.1984.0085

Cited by 318 publications

(71 citation statements)

References 22 publications

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“…In contrast, a different type of amacrine cell branching only in the off-sublamina may mediate the spatially offset inhibition that distinguishes the offresponses from the on-responses. A change in the timing of the off-inhibition in the preferred and null directions predicts a spatial offset of ϳ160 m, which is approximately half the dendritic diameter of a starburst cell in mid-peripheral retina (Tauchi and Masland, 1984;Vaney, 1984).…”

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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Section: Implications For Synaptic Circuitrymentioning

confidence: 99%

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

2002

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“…Type a cells have perikarya in the inner nuclear layer, processes ramifying in the outer half of the inner plexiform layer (IPL) in stratum 2 (S2) and OFF responses to light. Type b cells have perikarya displaced to the ganglion cell layer, processes ramifying in stratum 4 (S4) of the IPL and ON responses to light (Famiglietti, 1983;Tauchi and Masland, 1984;Vaney, 1984;Bloomfield and Miller, 1986). In rabbits, starburst amacrine cells are known to receive synaptic inputs from cone (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).…”

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confidence: 99%

AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

Firth

Massey

et al. 2003

J of Comparative Neurology

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The light response of starburst amacrine cells is initiated by glutamate released from bipolar cells. To identify the receptors that mediate this response, we used a combination of anatomical and physiological techniques. An in vivo, rabbit eyecup was preloaded with [ 3 H]-choline, and the [ 3 H]-acetylcholine (ACh) released into the superfusate was monitored. A photopic, 3 Hz flashing light increased ACh release, and the selective AMPA receptor antagonist, GYKI 53655, blocked this light-evoked response. Nonselective AMPA/kainate agonists increased the release of ACh, but the specific kainate receptor agonist, SYM 2081, did not increase ACh release. Selective AMPA receptor antagonists, GYKI 53655 or GYKI 52466, also blocked the responses to agonists. We conclude that the predominant excitatory input to starburst amacrine cells is mediated by AMPA receptors. We also labeled lightly fixed rabbit retinas with antisera to choline acetyltransferase (ChAT), AMPA receptor subunits GluR1, GluR2/3, or GluR4, and kainate receptor subunits GluR6/7 and KA2. Labeled puncta were observed in the inner plexiform layer with each of these antisera to glutamate receptors, but only GluR2/3-IR puncta and GluR4-IR puncta were found on the ChAT-IR processes. The same was true of starburst cells injected intracellularly with Neurobiotin, and these AMPA receptor subunits were localized to two populations of puncta. The AMPA receptors are expected to desensitize rapidly, enhancing the sensitivity of starburst amacrine cells to moving or other rapidly changing stimuli. Indexing termsglutamate; ionotropic receptors; localization; cholinergic; interneuron; confocal microscopy Starburst amacrine cells are one of the most common types of amacrine cells in rabbit retina (MacNeil et al., 1999), and there are two subtypes. Type a cells have perikarya in the inner nuclear layer, processes ramifying in the outer half of the inner plexiform layer (IPL) in stratum 2 (S2) and OFF responses to light. Type b cells have perikarya displaced to the ganglion cell layer, processes ramifying in stratum 4 (S4) of the IPL and ON responses to light (Famiglietti, 1983;Tauchi and Masland, 1984;Vaney, 1984;Bloomfield and Miller, 1986). In rabbits, starburst amacrine cells are known to receive synaptic inputs from cone (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).Starburst amacrine cells synthesize and release both γ-aminobutyric acid (GABA) and acetylcholine (ACh) when depolarized (Masland and Livingstone, 1976;Massey and Neal, 1979;O'Malley and Masland, 1989). ACh release from the rabbit retina increases at both light onset and light offset and is maximally stimulated by large stimuli at temporal frequencies of 1-4 Hz (Massey and Neal, 1979;Massey and Redburn, 1985;O'Malley and Masland, 1993). The majority of the synaptic output from the starburst cells is onto ganglion cell dendrites (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991 . The agonist α-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) is more potent than kainate or...

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“…Cholinergic amacrine cells, also known as starburst amacrine cells due to their unique morphology, form two mirror symmetric populations on either side of the inner plexiform layer (Vaney, 1984;Tauchi & Masland, 1984;Rodieck & Marshak, 1992). The cells in the inner nuclear layer produce OFF responses and stratify in sublamina a while the displaced starburst amacrine cells are ON cells branching in sublamina b.…”

Section: Introductionmentioning

confidence: 99%

Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

Zhang

Hoshi

et al. 2005

Vis Neurosci

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The correlation between cholinergic sensitivity and the level of stratification for ganglion cells was examined in the rabbit retina. As examples, we have used ON or OFF α ganglion cells and ON/OFF directionally selective (DS) ganglion cells. Nicotine, a cholinergic agonist, depolarized ON/OFF DS ganglion cells and greatly enhanced their firing rates but it had modest excitatory effects on ON or OFF α ganglion cells. As previously reported, we conclude that DS ganglion cells are the most sensitive to cholinergic drugs. Confocal imaging showed that ON/OFF DS ganglion cells ramify precisely at the level of the cholinergic amacrine cell dendrites, and co-fasciculate with the cholinergic matrix of starburst amacrine cells. However, neither ON or OFF α ganglion cells have more than a chance association with the cholinergic matrix. Z-axis reconstruction showed that OFF α ganglion cells stratify just below the cholinergic band in sublamina a while ON α ganglion cells stratify just below cholinergic b. The latter is at the same level as the terminals of calbindin bipolar cells. Thus, the calbindin bipolar cell appears to be a prime candidate to provide the bipolar cell input to ON α ganglion cells in the rabbit retina. We conclude that the precise level of stratification is correlated with the strength of cholinergic input. Alpha ganglion cells receive a weak cholinergic input and they are narrowly stratified just below the cholinergic bands.

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The shape and arrangement of the cholinergic neurons in the rabbit retina

Cited by 318 publications

References 22 publications

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

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