ON Inputs to the OFF Layer: Bipolar Cells That Break the Stratification Rules of the Retina

Hoshi, Hideo; Liu, Weili; Massey, Stephen C.; Mills, Steven

doi:10.1523/jneurosci.0912-09.2009

Cited by 123 publications

(197 citation statements)

References 37 publications

(63 reference statements)

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“…First, CBb4 3116 forms an axonal ribbon dyad onto bsdGC 15796 and a currently unidentified target (Figure 6 A,E). bsdGCs were identified in rabbit with dendrites that rise through the ON layer to stratify in the OFF IPL, where they receive CBb axonal ribbon input before re-entering the ON IPL (Hoshi et al, 2009). Our bsdGCs may be the same as the G9 ganglion cell identified by (Roska and Werblin, 2003), with depolarizing responses to light blocked by L-APB and enhanced by glycine and GABA receptor antagonists, and thus appear to be directly excited by ON cone bipolar cell input despite multistratification in both the ON and OFF IPL.…”

Section: Ganglion Cell Targetsmentioning

confidence: 99%

“…(Famiglietti et al, 1977;Famiglietti and Kolb, 1976;MacNeil et al, 2004;Wässle et al, 2009;Werblin and Dowling, 1969). Nevertheless, examples of nominal cone bipolar cells breaking the mammalian IPL stratification rules were recently reported (Anderson et al, 2011a;Dumitrescu et al, 2009;Hoshi et al, 2009). Type 6, and possibly type 7 or 8, ON cone bipolar cells in mouse, and calbindin-positive layer 4/5 stratifying ON cone bipolar cells in rabbit, have been demonstrated targeting tyrosine hydrdoxylasepositive cells (TH1s), M1-type intrinsically photosensitive retinal ganglion cells (ipRGCs) and bsdGCs in stratum one of the IPL (Dumitrescu et al, 2009;Hoshi et al, 2009), thus representing an accessory ON input to the OFF IPL layers.…”

Section: Introductionmentioning

confidence: 99%

“…Nevertheless, examples of nominal cone bipolar cells breaking the mammalian IPL stratification rules were recently reported (Anderson et al, 2011a;Dumitrescu et al, 2009;Hoshi et al, 2009). Type 6, and possibly type 7 or 8, ON cone bipolar cells in mouse, and calbindin-positive layer 4/5 stratifying ON cone bipolar cells in rabbit, have been demonstrated targeting tyrosine hydrdoxylasepositive cells (TH1s), M1-type intrinsically photosensitive retinal ganglion cells (ipRGCs) and bsdGCs in stratum one of the IPL (Dumitrescu et al, 2009;Hoshi et al, 2009), thus representing an accessory ON input to the OFF IPL layers. These ribbon contacts appear in two varieties: en passant, occurring inside the main bipolar cell descending axons, and branched, occurring from small processes that branch off the main descending axon ( Figure 2).…”

Section: Introductionmentioning

confidence: 99%

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ON cone bipolar cell axonal synapses in the OFF inner plexiform layer of the rabbit retina

Lauritzen

Anderson

Jones

et al. 2013

J of Comparative Neurology

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Analysis of the rabbit retinal connectome RC1 reveals that the division between the ON and OFF inner plexiform layer (IPL) is not structurally absolute. ON cone bipolar cells make non-canonical axonal synapses onto specific targets and receive amacrine cell synapses in the nominal OFF layer, creating novel motifs, including inhibitory crossover networks. Automated transmission electron microscope (ATEM) imaging, molecular tagging, tracing, and rendering of ≈ 400 bipolar cells reveals axonal ribbons in 36% of ON cone bipolar cells, throughout the OFF IPL. The targets include GABA-positive amacrine cells (γACs), glycine-positive amacrine cells (GACs) and ganglion cells. Most ON cone bipolar cell axonal contacts target GACs driven by OFF cone bipolar cells, forming new architectures for generating ON-OFF amacrine cells. Many of these ON-OFF GACs target ON cone bipolar cell axons, ON γACs and/or ON-OFF ganglion cells, representing widespread mechanisms for OFF to ON crossover inhibition. Other targets include OFF γACs presynaptic to OFF bipolar cells, forming γAC-mediated crossover motifs. ON cone bipolar cell axonal ribbons drive bistratified ON-OFF ganglion cells in the OFF layer and provide ON drive to polarity-appropriate targets such as bistratified diving ganglion cells (bsdGCs). The targeting precision of ON cone bipolar cell axonal synapses shows that this drive incidence is necessarily a joint distribution of cone bipolar cell axonal frequency and target cell trajectories through a given volume of the OFF layer. Such joint distribution sampling is likely common when targets are sparser than sources and when sources are coupled, as are ON cone bipolar cells.

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Section: Ganglion Cell Targetsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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ON cone bipolar cell axonal synapses in the OFF inner plexiform layer of the rabbit retina

Lauritzen

Anderson

Jones

et al. 2013

J of Comparative Neurology

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“…DA cells are interplexiform cells and play a major role in retinal light adaptation (Witkovsky, 2004). Recently, DA cells have been shown to receive inputs via en passant synapses from ON bipolar cells (Dumitrescu et al, 2009;Hoshi et al, 2009) and via a centrifugal pathway from melanopsinexpressing ganglion cells (Zhang et al, 2008). In contrast, inputs to type 2 cells have only been described on the ultrastructural level in the monkey retina (Mariani, 1991).…”

Section: Introductionmentioning

confidence: 99%

Inputs Underlying the ON–OFF Light Responses of Type 2 Wide-Field Amacrine Cells in TH::GFP Mice

Knop

Feigenspan²,

Weiler³

et al. 2011

J. Neurosci.

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“…The anatomical basis for this very unusual ON physiological input to M1 ipRGCs with dendrites in the OFF sublayer of the IPL appears to be mediated by ectopic synapses onto M1 ipRGCs from ON-bipolar cells as their axons pass through the OFF layer of the IPL (Fig. 1) (Dumitrescu et al 2009;Hoshi et al 2009). This arrangement has been described as an accessory ON sublayer in the outer IPL (Dumitrescu et al 2009).…”

Section: Different Types Of Iprgc Have Different Central Targetsmentioning

confidence: 99%

Intrinsically photosensitive retinal ganglion cells

Pickard

Sollars

2010

Sci. China Life Sci.

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Intrinsically photosensitive retinal ganglion cells (ipRGCs) respond to light in the absence of all rod and cone photoreceptor input. The existence of these ganglion cell photoreceptors, although predicted from observations scattered over many decades, was not established until it was shown that a novel photopigment, melanopsin, was expressed in retinal ganglion cells of rodents and primates. Phototransduction in mammalian ipRGCs more closely resembles that of invertebrate than vertebrate photoreceptors and appears to be mediated by transient receptor potential channels. In the retina, ipRGCs provide excitatory drive to dopaminergic amacrine cells and ipRGCs are coupled to GABAergic amacrine cells via gap junctions. Several subtypes of ipRGC have been identified in rodents based on their morphology, physiology and expression of molecular markers. ipRGCs convey irradiance information centrally via the optic nerve to influence several functions including photoentrainment of the biological clock located in the hypothalamus, the pupillary light reflex, sleep and perhaps some aspects of vision. In addition, ipRGCs may also contribute irradiance signals that interface directly with the autonomic nervous system to regulate rhythmic gene activity in major organs of the body. Here we review the early work that provided the motivation for searching for a new mammalian photoreceptor, the ground-breaking discoveries, current progress that continues to reveal the unusual properties of these neuron photoreceptors, and directions for future investigation.Keywords: Melanopsin, Circadian rhythms, Suprachiasmatic nucleus, Retina digitalcommons.unl.edu P i c k a r d & S o l l a r S i n R e v P h y s i o l B i o c h e m P h a R m a c o l1 6 2 ( 2 0 1 2 ) Early Hints of a Third Photoreceptor in the Mammalian RetinaThe perception of shapes, color and objects moving in the world begins in the outer retina where light is absorbed by photopigments that are integral membrane apoproteins (opsins) covalently linked to a retinaldehyde chromophore in the rod and cone photoreceptors. The capturing of photons by rod and cone photoreceptors initiates a signaling cascade in which photon capture is converted into an electrical signal. The simplest common pathway these signals take from the eye to the brain is from the photoreceptors to bipolar cells to ganglion cells. Retinal ganglion cells (RGCs) convey the signals centrally as action potentials, transmitted via their axons in the optic nerve, to higher brain regions for integration and the further processing required for conscious visual perception (Fig. 1). Among non-mammalian vertebrates, photoreceptors are also found in locations outside the retina, including the pineal gland and in the brain itself. These extra-ocular photoreceptors mediate tasks not associated directly with visual perception (non-image forming functions such as hormone regulation). However, since the pioneering descriptions of the vertebrate retina by Santiago Ramón y Cajal in the late 1800s, it was believed that t...

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ON Inputs to the OFF Layer: Bipolar Cells That Break the Stratification Rules of the Retina

Cited by 123 publications

References 37 publications

ON cone bipolar cell axonal synapses in the OFF inner plexiform layer of the rabbit retina

ON cone bipolar cell axonal synapses in the OFF inner plexiform layer of the rabbit retina

Inputs Underlying the ON–OFF Light Responses of Type 2 Wide-Field Amacrine Cells in TH::GFP Mice

Intrinsically photosensitive retinal ganglion cells

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