GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina

Ackert, Jessica; Farajian, Reza; Völgyi, Béla; Bloomfield, Stewart A.

doi:10.1113/jphysiol.2009.173344

Cited by 52 publications

(96 citation statements)

References 68 publications

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“…Together these results indicate that BCs terminating at a similar IPL depth may form different functional circuits and have different receptive fields. For example, ON and ON-OFF DSGCs ramify at a similar depth of sublamina b (Ackert et al 2009;Dong et al 2004;Sun et al 2006) but receive kinetically different glutamate inputs and have very different light response kinetics and speed tuning properties (Ackert et al 2009;Ariel and Daw 1982;Sivyer et al 2010;Weng et al 2005). Future studies will determine whether CB5 1 and CB5 2 preferentially target one over the other type of DSGC.…”

Section: Discussionmentioning

confidence: 94%

Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

Chen

Lee

Park

et al. 2014

Journal of Neurophysiology

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Retinal bipolar cells (BCs) transmit visual signals in parallel channels from the outer to the inner retina, where they provide glutamatergic inputs to specific networks of amacrine and ganglion cells. Intricate network computation at BC axon terminals has been proposed as a mechanism for complex network computation, such as direction selectivity, but direct knowledge of the receptive field property and the synaptic connectivity of the axon terminals of various BC types is required in order to understand the role of axonal computation by BCs. The present study tested the essential assumptions of the presynaptic model of direction selectivity at axon terminals of three functionally distinct BC types that ramify in the direction-selective strata of the mouse retina. Results from two-photon Ca(2+) imaging, optogenetic stimulation, and dual patch-clamp recording demonstrated that 1) CB5 cells do not receive fast GABAergic synaptic feedback from starburst amacrine cells (SACs); 2) light-evoked and spontaneous Ca(2+) responses are well coordinated among various local regions of CB5 axon terminals; 3) CB5 axon terminals are not directionally selective; 4) CB5 cells consist of two novel functional subtypes with distinct receptive field structures; 5) CB7 cells provide direct excitatory synaptic inputs to, but receive no direct GABAergic synaptic feedback from, SACs; and 6) CB7 axon terminals are not directionally selective, either. These findings help to simplify models of direction selectivity by ruling out complex computation at BC terminals. They also show that CB5 comprises two functional subclasses of BCs.

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Section: Discussionmentioning

confidence: 94%

Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

Chen

Lee

Park

et al. 2014

Journal of Neurophysiology

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“…A recent report by Lee et al (2006) showed that nicotinic ACh transmission is implicated in direction selectivity. Moreover, Ackert et al (2009) suggest a role for ACh in generating the OFF responses in ON DSGCs. The existence of cholinergic amacrine cells in the zebrafish retina has been shown by several groups (Yazulla and Studholme, 2001;Arenzana et al, 2005); their functional analogy to Starburst amacrine cells of the mammalian retina, however, has not been established.…”

Section: Discussionmentioning

confidence: 99%

Distinct Retinal Deficits in a Zebrafish Pyruvate Dehydrogenase-Deficient Mutant

2010

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Mutations in ubiquitously expressed metabolic genes often lead to CNS-specific effects, presumably because of the high metabolic demands of neurons. However, mutations in omnipresent metabolic pathways can conceivably also result in cell type-specific effects because of cell-specific requirements for intermediate products. One such example is the zebrafish noir mutant, which we found to be mutated in the pdhb gene, coding for the E1 ␤ subunit of the pyruvate dehydrogenase complex. This vision mutant is described as blind and was isolated because of its vision defect-related darker appearance. A detailed morphological, behavioral, and physiological analysis of the phenotype revealed an unexpected specific effect on the retina. Surprisingly, the cholinergic amacrine cells of the inner retina are affected earlier than the photoreceptors. This might be attributable to the inability of these cells to maintain production of their neurotransmitter acetylcholine. This is reflected in an earlier loss of motion vision, followed only later by a general loss of light perception. Since both characteristics of the phenotype are attributable to a loss of acetyl-CoA production by pyruvate dehydrogenase, we used a ketogenic diet to bypass this metabolic block and could indeed partially rescue vision and prolong survival of the larvae. The noir mutant provides a case for a systemic disease with ocular manifestation with a surprising specific effect on the retina given the ubiquitous requirement for the mutated gene.

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“…Surprisingly, the unmasked OFF response is also direction selective, showing a preferred direction opposite to that of the ON response 71,72 (but see 70 ). The detailed mechanisms underlying the unmasked OFF response are still not clear, but are known to depend on gap junction coupling between ON DSGCs and a class of polyaxonal amacrine cells 71,72 . Another set of studies 73,74 imply heterogeneity of ON DSGCs.…”

Section: Synaptic Mechanisms and Development Of Other Dsgc Typesmentioning

confidence: 98%

Section: Synaptic Mechanisms and Development Of Other Dsgc Typesmentioning

confidence: 99%

“…72 A recent study found that application of GABA A receptor antagonist picrotoxin unmasks an OFF spiking response in ON DSGCs, in addition to disrupting the direction selectivity of the ON responses. Surprisingly, the unmasked OFF response is also direction selective, showing a preferred direction opposite to that of the ON response 71,72 (but see 70 ). The detailed mechanisms underlying the unmasked OFF response are still not clear, but are known to depend on gap junction coupling between ON DSGCs and a class of polyaxonal amacrine cells 71,72 .…”

Section: Synaptic Mechanisms and Development Of Other Dsgc Typesmentioning

confidence: 99%

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Organization and development of direction-selective circuits in the retina

Wei

Feller

2011

Trends in Neurosciences

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The direction selective circuit in the retina extracts the directional information of image motion in the visual scene. It is a classic model for neural circuit analysis because its input and output are well-defined and accessible to physiological measurements. However, the neural basis of direction selectivity is still not fully understood. Indeed, this ostensibly simple computation arises from a collection of complex neural mechanisms at all levels of circuit organization. In this review, we describe recent advances in genetic, imaging and optogenetic techniques that have improved our understanding of the synaptic organization and development underlying retinal direction selectivity.

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GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina

Cited by 52 publications

References 68 publications

Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

Distinct Retinal Deficits in a Zebrafish Pyruvate Dehydrogenase-Deficient Mutant

Organization and development of direction-selective circuits in the retina

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