The Effect of PKCα on the Light Response of Rod Bipolar Cells in the Mouse Retina

Light decrements are mediated by two distinct groups of rod pathways in the dark-adapted retina that can be differentiated on the basis of their sensitivity to the glutamate agonist DL-2-amino-phosphonobutyric (APB). By means of the APB sensitive pathway, rods transmit light decrementsviarod bipolar cells to AII amacrine cells, then to Off cone bipolar cells, which in turn innervate the dendrites of Off ganglion cells. APB hyperpolarizes rod bipolar cells, thus blocking this rod pathway. With APB insensitive pathways, rods either directly synapse onto Off cone bipolar cells, or rods pass light decrement signal to cones by gap junctions. In the present study, whole-cell patch-clamp recordings were made from ganglion cells in the dark-adapted mouse retina to investigate the functional properties of APB sensitive and insensitive rod pathways. The results revealed several clear-cut differences between the APB sensitive and APB insensitive rod pathways. The latency of Off responses to a flashing spot of light was significantly shorter for the APB insensitive pathways than those for the APB sensitive pathway. Moreover, Off responses of the APB insensitive pathways were found to be capable of following substantially higher stimulus frequencies. Nitric oxide was found to selectively block Off responses in the APB sensitive rod pathway. Collectively, these results provide evidence that the APB sensitive and insensitive rod pathways can convey different types of information signaling light decrements in the dark-adapted retina.

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A group I metabotropic glutamate receptor controls synaptic gain between rods and rod bipolar cells in the mouse retina

Physiological Reports ◽

10.14814/phy2.13885 ◽

2018 ◽

Vol 6 (20) ◽

pp. e13885

Author(s):

Chase B. Hellmer ◽

Melissa Rampino Clemons ◽

Scott Nawy ◽

Tomomi Ichinose

Keyword(s):

Glutamate Receptor ◽

Metabotropic Glutamate Receptor ◽

Bipolar Cells ◽

Mouse Retina ◽

Metabotropic Glutamate ◽

Group I ◽

Synaptic Gain ◽

Rod Bipolar Cells

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Inhibitory Feedback Shapes Bipolar Cell Responses in the Rabbit Retina

Journal of Neurophysiology ◽

10.1152/jn.00838.2007 ◽

2007 ◽

Vol 98 (6) ◽

pp. 3423-3435 ◽

Cited By ~ 44

Author(s):

Alyosha Molnar ◽

Frank Werblin

Keyword(s):

Bipolar Cell ◽

Light Response ◽

Bipolar Cells ◽

Inhibitory Input ◽

Rabbit Retina ◽

Cell Responses ◽

Inhibitory Feedback ◽

Glycinergic Inhibition ◽

Rod Bipolar Cells ◽

Cone Bipolar Cells

Retinal bipolar cells can be divided into on and off types based on the polarity of their response to light. Bipolar activity is further shaped by inhibitory inputs, characterized here by the events that occur immediately after the onset of a light step: 1) in most off bipolar cells, excitatory current decreased, whereas inhibitory current increased. These currents reinforced each other, enhancing the light response. 2) In about half of the on cone bipolar cells, the excitatory current increased, whereas inhibitory current decreased, also reinforcing the light response. Both of these reinforcing interactions were mediated by glycinergic inhibition. 3) In the remaining on cone bipolar cells, excitation and inhibition both increased, but inhibition was delayed so that these cells responded transiently. 4) Finally, in rod bipolar cells, excitation and inhibition both increased so that inhibition suppressed excitation, reducing the light response at all time scales. The suppressive inhibition seen in on cone and rod bipolar cells was mediated by GABA. Thus morphologically diverse bipolar cells receive only four main types of inhibitory input, and the majority of “inhibitory” inputs actually serve to enhance excitation.

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Cross-synaptic synchrony and transmission of signal and noise across the mouse retina

eLife ◽

10.7554/elife.03892 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 16

Author(s):

William N Grimes ◽

Mrinalini Hoon ◽

Kevin L Briggman ◽

Rachel O Wong ◽

Fred Rieke

Keyword(s):

Single Neuron ◽

Amacrine Cells ◽

Light Level ◽

Bipolar Cells ◽

Mouse Retina ◽

Anatomical Connectivity ◽

Physiological Conditions ◽

Synaptic Noise ◽

Mammalian Retina ◽

Rod Bipolar Cells

Cross-synaptic synchrony—correlations in transmitter release across output synapses of a single neuron—is a key determinant of how signal and noise traverse neural circuits. The anatomical connectivity between rod bipolar and A17 amacrine cells in the mammalian retina, specifically that neighboring A17s often receive input from many of the same rod bipolar cells, provides a rare technical opportunity to measure cross-synaptic synchrony under physiological conditions. This approach reveals that synchronization of rod bipolar cell synapses is near perfect in the dark and decreases with increasing light level. Strong synaptic synchronization in the dark minimizes intrinsic synaptic noise and allows rod bipolar cells to faithfully transmit upstream signal and noise to downstream neurons. Desynchronization in steady light lowers the sensitivity of the rod bipolar output to upstream voltage fluctuations. This work reveals how cross-synaptic synchrony shapes retinal responses to physiological light inputs and, more generally, signaling in complex neural networks.

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Depolarizing effect of GABA in rod bipolar cells of the mouse retina

Vision Research ◽

10.1016/j.visres.2005.03.020 ◽

2005 ◽

Vol 45 (20) ◽

pp. 2659-2667 ◽

Cited By ~ 31

Author(s):

Carolina Varela ◽

Román Blanco ◽

Pedro De la Villa

Keyword(s):

Bipolar Cells ◽

Mouse Retina ◽

Rod Bipolar Cells

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Localization of protein kinase C to UV-sensitive photoreceptors in the mouse retina

Visual Neuroscience ◽

10.1017/s0952523898151155 ◽

1998 ◽

Vol 15 (1) ◽

pp. 87-95 ◽

Cited By ~ 10

Author(s):

K.C. WIKLER ◽

D.L. STULL ◽

B.E. REESE ◽

P.T. JOHNSON ◽

E. BOGENMANN

Keyword(s):

Protein Kinase C ◽

Protein Kinase ◽

Regulatory Elements ◽

Bipolar Cells ◽

Mouse Retina ◽

Transcriptional Regulatory Elements ◽

Kinase C ◽

Transcriptional Regulatory ◽

Double Label ◽

Rod Bipolar Cells

The present study has identified a population of cone photoreceptors in the murine retina that are uniquely immunoreactive for protein kinase C (PKC). Wavelength-sensitive cone subtypes are segregated along the dorso-ventral axis in the mouse retina with ventral retina occupied exclusively by ultraviolet wavelength-sensitive (UVWS) cones, and dorsal retina dominated by middle wavelength-sensitive cones. PKC-positive cones are found primarily in the ventral retina, and double-label immunocytochemistry using a short wavelength-sensitive opsin antibody confirms that they specifically correspond to the UVWS cone subtype. The PKC antibody, as documented in other mammals, also identifies rod bipolar cells in the mouse retina. UVWS cones and bipolar cells have previously been shown to share transcriptional regulatory elements, as observed in transgenic mice encoding a portion of the human SWS-opsin promoter controlling the lacZ reporter gene. In such mice, the transgene product, β-galactosidase, is expressed in populations of both cones and bipolar cells. The present study confirms that lacZ-expressing photoreceptors are indeed PKC-positive photoreceptors, but that the lacZ-expressing bipolar cells are not the PKC-positive rod bipolar cells. These cells must correspond to a type of cone bipolar cell.

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Reconvergence of a rod signal to an AII amacrine cell through divergence to a pair of rod bipolar cells in the mouse retina

Neuroscience Research ◽

10.1016/j.neures.2011.07.293 ◽

2011 ◽

Vol 71 ◽

pp. e69

Author(s):

Yoshihiko Tsukamoto ◽

Naoko Omi

Keyword(s):

Amacrine Cell ◽

Bipolar Cells ◽

Mouse Retina ◽

Rod Bipolar Cells ◽

Aii Amacrine

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Coordinated control of sensitivity by two splice variants of Gαo in retinal ON bipolar cells

The Journal of General Physiology ◽

10.1085/jgp.201010477 ◽

2010 ◽

Vol 136 (4) ◽

pp. 443-454 ◽

Cited By ~ 19

Author(s):

Haruhisa Okawa ◽

Johan Pahlberg ◽

Fred Rieke ◽

Lutz Birnbaumer ◽

Alapakkam P. Sampath

Keyword(s):

G Protein ◽

Single Photon ◽

Splice Variants ◽

Light Response ◽

Light Sensitivity ◽

Bipolar Cells ◽

Protein Activity ◽

Α Subunit ◽

Coordinated Action ◽

Rod Bipolar Cells

The high sensitivity of scotopic vision depends on the efficient retinal processing of single photon responses generated by individual rod photoreceptors. At the first synapse in the mammalian retina, rod outputs are pooled by a rod “ON” bipolar cell, which uses a G-protein signaling cascade to enhance the fidelity of the single photon response under conditions where few rods absorb light. Here we show in mouse rod bipolar cells that both splice variants of the Go α subunit, Gαo1 and Gαo2, mediate light responses under the control of mGluR6 receptors, and their coordinated action is critical for maximizing sensitivity. We found that the light response of rod bipolar cells was primarily mediated by Gαo1, but the loss of Gαo2 caused a reduction in the light sensitivity. This reduced sensitivity was not attributable to the reduction in the total number of Go α subunits, or the altered balance of expression levels between the two splice variants. These results indicate that Gαo1 and Gαo2 both mediate a depolarizing light response in rod bipolar cells without occluding each other’s actions, suggesting they might act independently on a common effector. Thus, Gαo2 plays a role in improving the sensitivity of rod bipolar cells through its action with Gαo1. The coordinated action of two splice variants of a single Gα may represent a novel mechanism for the fine control of G-protein activity.

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