Center surround receptive field structure of cone bipolar cells in primate retina

Dacey, Dennis M.; Packer, Orin S.; Diller, Lisa C.; Brainard, David H.; Peterson, Barry T.; Lee, Barry

doi:10.1016/s0042-6989(00)00039-0

Cited by 195 publications

(190 citation statements)

References 49 publications

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“…Consistent with this interpretation, primate diffuse bipolar cells have center-surround receptive fields (Dacey et al, 2000a). Our results with L-AP4, however, are inconsistent with a complete separation of the ON and OFF pathways.…”

Section: Receptive Field Organizationsupporting

confidence: 56%

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Functional polarity of dendrites and axons of primate A1 amacrine cells

2007

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The A1 cell is an axon-bearing amacrine cell of the primate retina with a diffusely stratified, moderately branched dendritic tree (~400 µm diameter). Axons arise from proximal dendrites forming a second concentric, larger arborization (>4 mm diameter) of thin processes with boutonlike swellings along their length. A1 cells are ON-OFF transient cells that fire a brief high frequency burst of action potentials in response to light (Stafford & Dacey, 1997). It has been hypothesized that A1 cells receive local input to their dendrites, with action potentials propagating output via the axons across the retina, serving a global inhibitory function. To explore this hypothesis we recorded intracellularly from A1 cells in an in vitro macaque monkey retina preparation. A1 cells have an antagonistic center-surround receptive field structure for the ON and OFF components of the light response. Blocking the ON pathway with L-AP4 eliminated ON center responses but not OFF center responses or ON or OFF surround responses. Blocking GABAergic inhibition with picrotoxin increased response amplitudes without affecting receptive field structure. TTX abolished action potentials, with little effect on the sub-threshold light response or basic receptive field structure. We also used multi-photon laser scanning microscopy to record light-induced calcium transients in morphologically identified dendrites and axons of A1 cells. TTX completely abolished such calcium transients in the axons but not in the dendrites. Together these results support the current model of A1 function, whereby the dendritic tree receives synaptic input that determines the center-surround receptive field; and action potentials arise in the axons, which propagate away from the dendritic field across the retina.

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Section: Receptive Field Organizationsupporting

confidence: 56%

“…Primate cone bipolar cells have center-surround receptive field structure (Dacey et al, 2000a). ON cone bipolar cells have an ON center response that is antagonized by simultaneous surround stimulation.…”

Section: A1 Center-surround Receptive Field Structurementioning

confidence: 99%

Functional polarity of dendrites and axons of primate A1 amacrine cells

2007

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“…The third stimulus was a small spot (0.1 mm diameter) at higher contrast levels (0.1 or 0.3), which should generate a relatively small response in the ganglion cell but large responses in the centralmost approximately four bipolar cells. Here, we assumed that bipolar cells are spaced at ϳ30 m and have receptive fields of ϳ100 m (Dacey et al, 2000).…”

Section: Contrast Gain Control Does Not Require Inhibitory Synapsesmentioning

confidence: 99%

“…Such a synaptic mechanism would explain why one study found much stronger gain control in ganglion cell membrane potential than in bipolar cells, recorded in the same preparation (Baccus and Meister, 2002). Recordings of bipolar cells in the intact mammalian retina have been extremely limited, given the difficulty in obtaining stable recordings and identifying the bipolar cell type (Dacey et al, 2000). Here, we have shown that amacrine cell signaling is not critical for gain control, and therefore one could justify further study in the mammalian retinal slice, where identification of cone-bipolar cell types is more routine (Li and DeVries, 2006).…”

Section: Bipolar Cell Roles In Contrast Gain Control and Slow Contrasmentioning

confidence: 99%

Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells

Beaudoin¹,

Borghuis²,

Demb³

2007

J. Neurosci.

114

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Retinal ganglion cells fire spikes to an appropriate contrast presented over their receptive field center. These center responses undergo dynamic changes in sensitivity depending on the ongoing level of contrast, a process known as "contrast gain control." Extracellular recordings suggested that gain control is driven by a single wide-field mechanism, extending across the center and beyond, that depends on inhibitory interneurons: amacrine cells. However, recordings in salamander suggested that the excitatory bipolar cells, which drive the center, may themselves show gain control independently of amacrine cell mechanisms. Here, we tested in mammalian ganglion cells whether amacrine cells are critical for gain control over the receptive field center. We made extracellular and whole-cell recordings of guinea pig Y-type cells in vitro and quantified the gain change between contrasts using a linear-nonlinear analysis. For spikes, tripling contrast reduced gain by ϳ40%. With spikes blocked, ganglion cells showed similar levels of gain control in membrane currents and voltages and under conditions of low and high calcium buffering: tripling contrast reduced gain by ϳ20 -25%. Gain control persisted under voltage-clamp conditions that minimize inhibitory conductances and pharmacological conditions that block inhibitory neurotransmitter receptors. Gain control depended on adequate stimulation, not of ganglion cells but of presynaptic bipolar cells. Furthermore, horizontal cell measurements showed a lack of gain control in photoreceptor synaptic release. Thus, the mechanism for gain control over the ganglion cell receptive field center, as measured in the subthreshold response, originates in the presynaptic bipolar cells and does not require amacrine cell signaling.

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“…Antagonistic receptive field surrounds can be detected in mammalian bipolar cells (Dacey et al, 2000). GABA released from horizontal cells onto bipolar cell dendrites could participate in this process (Yang, 2004).…”

Section: Targets For Gaba Releasementioning

confidence: 99%

Cellular distribution and subcellular localization of molecular components of vesicular transmitter release in horizontal cells of rabbit retina

Hirano

Brandstätter

Brecha

2005

J of Comparative Neurology

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The mechanism underlying transmitter release from retinal horizontal cells is poorly understood. We investigated the possibility of vesicular transmitter release from mammalian horizontal cells by examining the expression of synaptic proteins that participate in vesicular transmitter release at chemical synapses. Using immunocytochemistry, we evaluated the cellular and subcellular distribution of complexin I/II, syntaxin-1, and synapsin I in rabbit retina. Strong labeling for complexin I/II, proteins that regulate a late step in vesicular transmitter release, was found in both synaptic layers of the retina, and in somata of A-and B-type horizontal cells, of ␥-aminobutyric acid (GABA)-and glycinergic amacrine cells, and of ganglion cells. Immunoelectron microscopy demonstrated the presence of complexin I/II in horizontal cell processes postsynaptic to rod and cone ribbon synapses. Syntaxin-1, a core protein of the soluble N-ethylmaleimide-sensitive-factor attachment protein receptor (SNARE) complex known to bind to complexin, and synapsin I, a synaptic vesicle-associated protein involved in the Ca 2ϩ -dependent recruitment of synaptic vesicles for transmitter release, were also present in the horizontal cells and their processes at photoreceptor synapses. Photoreceptors and bipolar cells did not express any of these proteins at their axon terminals. The presence of complexin I/II, syntaxin-1, and synapsin I in rabbit horizontal cell processes and tips suggests that a vesicular mechanism may underlie transmitter release from mammalian horizontal cells.

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Center surround receptive field structure of cone bipolar cells in primate retina

Cited by 195 publications

References 49 publications

Functional polarity of dendrites and axons of primate A1 amacrine cells

Functional polarity of dendrites and axons of primate A1 amacrine cells

Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells

Cellular distribution and subcellular localization of molecular components of vesicular transmitter release in horizontal cells of rabbit retina

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