Retinal resistance barriers and electrical lateral inhibition

Shaw, Stephen R.

doi:10.1038/255480a0

Cited by 108 publications

(48 citation statements)

References 20 publications

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“…In these conventional recordings, the potential difference in the dark between the extracellular space in the retina and the extracellular space within the lamina cartridge was Ϫ27.6 Ϯ 3.5 mV (n ϭ 21). This value did not depend on the direction in which the electrode approached the lamina (i.e., from retina or directly into the lamina via the back of the head capsule) and is within the range of previously published reports (Mote, 1970;Laughlin, 1974;Shaw, 1975).…”

Section: Measuring the Fp With Potassium Acetate Electrodessupporting

confidence: 64%

“…Three epithelial glial cells (EGC) form a sheath around the cartridge that encloses the extracellular space and restricts diffusion between neighboring cartridges (redrawn after Shaw, 1981Shaw, , 1984. B, Basic electrical circuit showing how current leaving photoreceptor terminals depolarizes the extracellular space in a lamina cartridge (redrawn after Shaw, 1975). The left-hand side of the circuit shows light-gated current entering the photoreceptor soma in the retina and leaving via its axon terminal in the lamina.…”

Section: Methodsmentioning

confidence: 99%

“…As originally demonstrated by Shaw (1975) in the locust eye, electrical isolation of the extracellular space of the first optic neuropile (the lamina) is a prerequisite for a large FP. The degree of isolation was measured by injecting small current pulses (Ϫ0.2 nA, 300 ms) into the extracellular space, via the recording electrode, and measuring the resultant polarization.…”

Section: The Synaptic Zone Is Electrically Isolated From the Hemolymphmentioning

confidence: 99%

“…Fish retinal horizontal cells have hemichannels, apparently capable of injecting current into the extracellular space of the cone pedicle to produce lateral inhibition and chromatic opponency in bipolar cells (Byzov and Trifonov, 1968;Byzov and Shura-Bura, 1986;Kamermans et al, 2001). Insect compound eyes exhibit large extracellular field potentials (FPs) (Mote, 1970) associated with resistance barriers surrounding photoreceptor axon terminals (Shaw, 1975(Shaw, , 1984, which could subtract redundant components by changing the presynaptic membrane potential (Laughlin, 1974(Laughlin, , 1981Shaw, 1978Shaw, , 1984Zimmerman, 1978) (see Fig. 1, schematic descriptions).…”

Section: Introductionmentioning

confidence: 99%

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Extracellular Potentials Modify the Transfer of Information at Photoreceptor Output Synapses in the Blowfly Compound Eye

Weckström

Laughlin²

2010

Journal of Neuroscience

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. The synapses are contained in compartments, lamina cartridges, whose extracellular potentials change with illumination (Shaw, 1984). We described these extracellular field potentials (FPs) using a novel permeabilization technique that converts neurons into extracellular recording probes. Having characterized extracellular FPs, we went on to study them using conventional microelectrodes. Extracellular space in a cartridge is electrically isolated from the body cavity and retina [input resistance (R in ) ϭ 6.0 M⍀ in dark], and light adaptation increases this isolation (R in ϭ 7.8 M⍀). In the dark, the extracellular space is 30 mV hyperpolarized compared with retina, and this promotes tonic synaptic activity by depolarizing the synaptic terminals. Illumination depolarizes the extracellular space, and voltage-clamp studies suggest that the postsynaptic chloride current in LMCs contributes to this light response. The presynaptic transmembrane potential in the photoreceptor axon was estimated by subtracting the FP from intracellular recordings. By backing off the presynaptic input, the FP can reset the synaptic operating range, produce response transients, and contribute to predictive coding by subtracting redundant low frequencies.

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Section: Measuring the Fp With Potassium Acetate Electrodessupporting

confidence: 64%

Section: Methodsmentioning

confidence: 99%

Section: The Synaptic Zone Is Electrically Isolated From the Hemolymphmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Extracellular Potentials Modify the Transfer of Information at Photoreceptor Output Synapses in the Blowfly Compound Eye

Weckström

Laughlin²

2010

Journal of Neuroscience

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“…The rather large scatter in the PS estimate may be due to our inability to determine the exact photoreceptor from which recordings were made (i.e. whether it was a small or large RC), potential electrical interactions between photoreceptors (Shaw 1975;Labhart 1980), and/or regional differences in possible microvillar misalignments (Nilsson et al 1987). According to theory, a perfect alignment of the rhodposin molecules within the microvilli would lead to a polarisation sensitivity maximum of 20 (Laughlin et al 1975).…”

Section: Discussionmentioning

confidence: 99%

Anatomical and physiological evidence for polarisation vision in the nocturnal bee Megalopta genalis

Greiner

Cronin²,

Ribi

et al. 2007

J Comp Physiol A

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The presence of a specialised dorsal rim area with an ability to detect the e-vector orientation of polarised light is shown for the first time in a nocturnal hymenopteran. The dorsal rim area of the halictid bee Megalopta genalis features a number of characteristic anatomical specialisations including an increased rhabdom diameter and a lack of primary screening pigments. Optically, these specialisations result in wide spatial receptive fields (Ap = 14°), a common adaptation found in the dorsal rim areas of insects used to filter out interfering effects (i.e. clouds) from the sky. In this specialised eye region all nine photoreceptors contribute their microvilli to the entire length of the ommatidia. These orthogonally directed microvilli are anatomically arranged in an almost linear, anterior-posterior orientation. Intracellular recordings within the dorsal rim area show very high polarisation sensitivity and a sensitivity peak within the ultraviolet part of the spectrum.

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Primitive, crustacean-like state of blood-brain barrier in the eye of the apterygote insectPetrobius (Archaeognatha) determined from uptake of fluorescent tracers

Shaw

Varney

1999

J. Neurobiol.

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Compound eyes of insects in 16 orders were tested for the presence of a blood–retina barrier (BRB) by injecting the hemolymph with Procion yellow, which was excluded from the eye in all Neoptera but not in two apterygotes. A primitive apterygote (Petrobius, Machilidae) was investigated further. Epifluorescence observations with small dyes Lucifer yellow (LY) and sulforhodamine 101 (SR) confirmed uptake by the eye within 3 min of injection. LY and SR both penetrated the eye, particularly the cornea, examined in sections. Uptake was quantified by microfluorometry, yielding entry half‐times (t1/2) of 1–1.4 min, fitting predictions for a model where tracer uptake is limited by passive diffusion. A much larger fluorescent dextran entered at a similar rate (t1/2 = 1.70 ± 0.77 min; n = 22), too fast to be diffusion‐limited, pointing to an active process, probably flushing of hemolymph through the retina. This is not an artifact associated with tracer injection and may be the natural result of circulatory pressures. Microfluorometry gave a first estimate of hemolymph volume (2.9% of body weight), of hemolymph mixing time (t0.95 = 77 min); the eyes' receptive fields were also determined. All results point to a primitive crustacean‐like condition in Petrobius, with open access of hemolymph to the eye and no BRB. An evolutionary hypothesis is suggested to explain how a primitive central nervous system barrier later extended to cut off the eye in Neoptera, in the face of access problems for respiratory gases and metabolites. © 1999 John Wiley & Sons, Inc. J Neurobiol 41: 452–470, 1999

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Retinal resistance barriers and electrical lateral inhibition

Cited by 108 publications

References 20 publications

Extracellular Potentials Modify the Transfer of Information at Photoreceptor Output Synapses in the Blowfly Compound Eye

Extracellular Potentials Modify the Transfer of Information at Photoreceptor Output Synapses in the Blowfly Compound Eye

Anatomical and physiological evidence for polarisation vision in the nocturnal bee Megalopta genalis

Primitive, crustacean-like state of blood-brain barrier in the eye of the apterygote insectPetrobius (Archaeognatha) determined from uptake of fluorescent tracers

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