Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Tsukamoto, Yoshihiko; Omi, Naoko

doi:10.3389/fnana.2014.00105

Cited by 46 publications

(60 citation statements)

References 47 publications

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“…Reasons for these pairings are described in detail in the Discussion. Since we have already described five OFF types (FMB, DB1, 2, 3a, and 3b) of (cone) bipolar cells in detail (Tsukamoto and Omi, 2014, 2015a), here we focus on six ON types (IMB, BB, DB4, DB5, DB6, and GB) of (cone) bipolar cells. Although, a rod bipolar (RB) cell is presented for comparison with cone bipolar cells, the RB type was not examined further in this study.…”

Section: Resultsmentioning

confidence: 99%

“…This animal was kindly donated by the psychophysical research group in the (former) Electrotechnical Laboratory of the Ministry of International Trade and Industry, Japan. This SSTEM series is the same as that used in previous studies by Tsukamoto and Omi (2014, 2015a), where the details of sample preparation were described. The procedure was performed in compliance with the Guide for the Care and Use of Experimental Animals (Hyogo College of Medicine).…”

Section: Methodsmentioning

confidence: 99%

“…In accordance with these studies, we measured the same variables from three-dimensionally reconstructed bipolar cells. The definitions of these three variables were explained pictorially in our previous article (Figure 3 in Tsukamoto and Omi, 2014). In addition, we used ultrastructural variables of bipolar synaptic contacts with photoreceptors, PG cells, and MG cells at the electron microscopic level to distinguish bipolar cell types.…”

Section: Methodsmentioning

confidence: 99%

“…Puthussery et al (2013) identified DB3b as a novel type distinct from DB3a (formerly DB3) based on immunological and electrophysiological properties, while Tsukamoto and Omi (2013, 2014) identified DB3b based on EM showing basal contacts with both rods and cones. In mice, three OFF types (3a, 3b, and 4) and one ON type (7) contact both rods and cones (Mataruga et al, 2007; Tsukamoto et al, 2007; Haverkamp et al, 2008; Tsukamoto and Omi, 2014). It is thus of interest to determine if this is a specialization specific to species heavily reliant on dark light conditions or if any primate ON bipolar cells also contact rods and cones to form mixed pathways.…”

Section: Introductionmentioning

confidence: 99%

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ON Bipolar Cells in Macaque Retina: Type-Specific Synaptic Connectivity with Special Reference to OFF Counterparts

Tsukamoto

Omi²

2016

Front. Neuroanat.

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To date, 12 macaque bipolar cell types have been described. This list includes all morphology types first outlined by Polyak (1941) using the Golgi method in the primate retina and subsequently identified by other researchers using electron microscopy (EM) combined with the Golgi method, serial section transmission EM (SSTEM), and immunohistochemical imaging. We used SSTEM for the rod-dense perifoveal area of macaque retina, reconfirmed ON (cone) bipolar cells to be classified as invaginating midget bipolar (IMB), diffuse bipolar (DB)4, DB5, DB6, giant bipolar (GB), and blue bipolar (BB) types, and clarified their type-specific connectivity. DB4 cells made reciprocal synapses with a kind of ON-OFF lateral amacrine cell, similar to OFF DB2 cells. GB cells contacted rods and cones, similar to OFF DB3b cells. Retinal circuits formed by GB and DB3b cells are thought to substantiate the psychophysical finding of fast rod signals in mesopic vision. DB6 cell output synapses were directed to ON midget ganglion (MG) cells at 70% of ribbon contacts, similar to OFF DB1 cells that directed 60% of ribbon contacts to OFF MG cells. IMB cells contacted medium- or long-wavelength sensitive (M/L-) cones but not short-wavelength sensitive (S-) cones, while BB cells contacted S-cones but not M/L-cones. However, IMB and BB dendrites had similar morphological architectures, and a BB cell contacting a single S-cone resembled an IMB cell. Thus, both IMB and BB may be the ON bipolar counterparts of the OFF flat midget bipolar (FMB) type, likewise DB4 of DB2, DB5 of DB3a, DB6 of DB1, and GB of DB3b OFF bipolar type. The ON DB plus GB, and OFF DB cells predominantly contacted M/L-cones and their outputs were directed mainly to parasol ganglion (PG) cells but also moderately to MG cells. BB cells directed S-cone-driven outputs almost exclusively to small bistratified ganglion (SBG) cells. Some FMB cells predominantly contacted S-cones and their outputs were directed to OFF MG cells. Thus, two-step synaptic connections largely narrowed down the S-cone component to SBG and some OFF MG cells. The other OFF MG cells, ON MG cells, and ON and OFF PG cells constructed M/L-cone dominant pathways.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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ON Bipolar Cells in Macaque Retina: Type-Specific Synaptic Connectivity with Special Reference to OFF Counterparts

Tsukamoto

Omi²

2016

Front. Neuroanat.

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“…In mouse, some rod bipolar cell dendrites contact cones, and some cone bipolar cells contact rods (Behrens et al, 2016; Hack et al, 1999; Tsukamoto et al, 2001); physiological studies confirm these connections (Pang et al, 2010). These aberrant connections are much less prevalent in primate retina (Tsukamoto and Omi, 2014; Tsukamoto and Omi, 2016); most notably, rod bipolar cells appear to exclusively contact rods. This clearer anatomical segregation of rod and cone signals in primate compared to mouse is an important consideration for the mechanistic basis of rod-cone interactions.…”

Section: Retinal Circuitry and Potential Sites Of Rod-cone Interactionsmentioning

confidence: 99%

Parallel Processing of Rod and Cone Signals: Retinal Function and Human Perception

Grimes

Songco-Aguas

Rieke

2018

Annu. Rev. Vis. Sci.

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We know a good deal about the operation of the retina when either rod or cone photoreceptors provide the dominant input (i.e. very dim or very bright conditions). However, we know much less about how the retina operates when rods and cones are co-active (intermediate lighting conditions—e.g. dusk). Such mesopic conditions span 20–30% of the light levels over which vision operates and encompass many situations in which vision is essential—e.g. driving at night. These lighting conditions are challenging because rod and cone signals differ substantially: rod responses are nearing saturation, while cone responses are weak and noisy. A rich history of perceptual studies can guide our investigation of how the retina operates under mesopic conditions, and in doing so provide a powerful opportunity to link general issues about parallel processing in neural circuits with computation and perception. We review some of the successes and challenges in understanding the retinal basis of perceptual rod-cone interactions.

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Connectivity between the OFF bipolar type DB3a and six types of ganglion cell in the marmoset retina

Masri

Percival

Koizumi

et al. 2015

J of Comparative Neurology

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Parallel visual pathways originate at the first synapse in the retina, where cones make connections with cone bipolar cells that in turn contact ganglion cells. There are more ganglion cell types than bipolar types, suggesting that there must be divergence from bipolar to ganglion cells. Here we analyze the contacts between an OFF bipolar type (DB3a) and six ganglion cell types in the retina of the marmoset monkey (Callithrix jacchus). Ganglion cells were transfected via particle-mediated gene transfer of an expression plasmid for the postsynaptic density 95-green fluorescent protein (PSD95-GFP), and DB3a cells were labeled via immunohistochemistry. Ganglion cell types that fully or partially costratified with DB3a cells included OFF parasol, OFF midget, broad thorny, recursive bistratified, small bistratified, and large bistratified cells. On average, the number of DB3a contacts to parasol cells (18 contacts per axon terminal) is higher than that to other ganglion cell types (between four and seven contacts). We estimate that the DB3a output to OFF parasol cells accounts for at least 30% of the total DB3a output. Furthermore, we found that OFF parasol cells receive approximately 20% of their total bipolar input from DB3a cells, suggesting that other diffuse bipolar types also provide input to OFF parasol cells. We conclude that DB3a cells preferentially contact OFF parasol cells but also provide input to other ganglion cell types.

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Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Cited by 46 publications

References 47 publications

ON Bipolar Cells in Macaque Retina: Type-Specific Synaptic Connectivity with Special Reference to OFF Counterparts

ON Bipolar Cells in Macaque Retina: Type-Specific Synaptic Connectivity with Special Reference to OFF Counterparts

Parallel Processing of Rod and Cone Signals: Retinal Function and Human Perception

Connectivity between the OFF bipolar type DB3a and six types of ganglion cell in the marmoset retina

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