scholarly journals The Rod Pathway of the Microbat Retina Has Bistratified Rod Bipolar Cells and Tristratified AII Amacrine Cells

2013 ◽  
Vol 33 (3) ◽  
pp. 1014-1023 ◽  
Author(s):  
B. Muller ◽  
E. Butz ◽  
L. Peichl ◽  
S. Haverkamp
2009 ◽  
Vol 101 (5) ◽  
pp. 2339-2347 ◽  
Author(s):  
Margaret Lin Veruki ◽  
Espen Hartveit

Gap junction channels constitute specialized intercellular contacts that can serve as electrical synapses. In the rod pathway of the retina, electrical synapses between AII amacrine cells express connexin 36 (Cx36) and electrical synapses between AII amacrines and on-cone bipolar cells express Cx36 on the amacrine side and Cx36 or Cx45 on the bipolar side. For physiological investigations of the properties and functions of these electrical synapses, it is highly desirable to have access to potent pharmacological blockers with selective and reversible action. Here we use dual whole cell voltage-clamp recordings of pairs of AII amacrine cells and pairs of AII amacrine and on-cone bipolar cells in rat retinal slices to directly measure the junctional conductance ( Gj) between electrically coupled cells and to study the effect of the drug meclofenamic acid (MFA) on Gj. Consistent with previous tracer coupling studies, we found that MFA reversibly blocked the electrical synapse currents in a concentration-dependent manner, with complete block at 100 μM. Whereas MFA evoked a detectable decrease in Gj within minutes of application, the time to complete block of Gj was considerably longer, typically 20–40 min. After washout, Gj recovered to 20–90% of the control level, but the time to maximum recovery was typically >1 h. These results suggest that MFA can be a useful drug to investigate the physiological functions of electrical synapses in the rod pathway, but that the slow kinetics of block and reversal might compromise interpretation of the results and that explicit monitoring of Gj is desirable.


2012 ◽  
Vol 107 (10) ◽  
pp. 2649-2659 ◽  
Author(s):  
A. Cyrus Arman ◽  
Alapakkam P. Sampath

The nervous system frequently integrates parallel streams of information to encode a broad range of stimulus strengths. In mammalian retina it is generally believed that signals generated by rod and cone photoreceptors converge onto cone bipolar cells prior to reaching the retinal output, the ganglion cells. Near absolute visual threshold a specialized mammalian retinal circuit, the rod bipolar pathway, pools signals from many rods and converges on depolarizing (AII) amacrine cells. However, whether subsequent signal flow to OFF ganglion cells requires OFF cone bipolar cells near visual threshold remains unclear. Glycinergic synapses between AII amacrine cells and OFF cone bipolar cells are believed to relay subsequently rod-driven signals to OFF ganglion cells. However, AII amacrine cells also make glycinergic synapses directly with OFF ganglion cells. To determine the route for signal flow near visual threshold, we measured the effect of the glycine receptor antagonist strychnine on response threshold in fully dark-adapted retinal cells. As shown previously, we found that response threshold for OFF ganglion cells was elevated by strychnine. Surprisingly, strychnine did not elevate response threshold in any subclass of OFF cone bipolar cell. Instead, in every OFF cone bipolar subclass strychnine suppressed tonic glycinergic inhibition without altering response threshold. Consistent with this lack of influence of strychnine, we found that the dominant input to OFF cone bipolar cells in darkness was excitatory and the response threshold of the excitatory input varied by subclass. Thus, in the dark-adapted mouse retina, the high absolute sensitivity of OFF ganglion cells cannot be explained by signal transmission through OFF cone bipolar cells.


2006 ◽  
Vol 23 (1) ◽  
pp. 127-135 ◽  
Author(s):  
GUO-YONG WANG

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.


1999 ◽  
Vol 16 (6) ◽  
pp. 1181-1189 ◽  
Author(s):  
STEPHEN C. MASSEY ◽  
STEPHEN L. MILLS

Electrical synapses or gap junctions occur between many retinal neurons. However, in most cases, the gap junctions have not been visualized directly. Instead, their presence has been inferred from tracer spread throughout the network of cells. Thus, tracer coupling is taken as a marker for the presence of gap junctions between coupled cells. AII amacrine cells are critical interneurons in the rod pathway of the mammalian retina. Rod bipolar cell output passes to AII amacrine cells, which in turn make conventional synapses with OFF cone bipolar cells and gap junctions with ON cone bipolar cells. Injections of biotinylated tracers into AII amacrine cells reveals coupling between the AII amacrine cell network and heterologous coupling with a variety of ON cone bipolar cells, including the calbindin-positive cone bipolar cell. To directly visualize gap junctions in this network, we prepared material for electron microscopy that was double labeled with antibodies to calretinin and calbindin to label AII amacrine cells and calbindin-positive cone bipolar cells, respectively. AII amacrine cells were postsynaptic to large vesicle-laden rod bipolar terminals, as previously reported. Gap junctions were identified between AII amacrine cells and calbindin-positive cone bipolar cell terminals identified by the presence of immunostaining and ribbon synapses. This represents direct confirmation of gap junctions between two different yet positively identified cells, which are tracer coupled, and provides additional evidence that tracer coupling with Neurobiotin indicates the presence of gap junctions. These results also definitively establish the presence of gap junctions between AII amacrine cells and calbindin bipolar cells which can therefore carry rod signals to the ON alpha ganglion cell.


2009 ◽  
Vol 26 (3) ◽  
pp. 287-296 ◽  
Author(s):  
KATHRYN E. KLUMP ◽  
AI-JUN ZHANG ◽  
SAMUEL M. WU ◽  
DAVID W. MARSHAK

AbstractA number of authors have observed amacrine cells containing high levels of immunoreactive parvalbumin in primate retinas. The experiments described here were designed to identify these cells morphologically, to determine their neurotransmitter, to record their light responses, and to describe the other cells that they contact. Macaque retinas were fixed in paraformaldehyde and labeled with antibodies to parvalbumin and one or two other markers, and this double- and triple-labeled material was analyzed by confocal microscopy. In their morphology and dendritic stratification patterns, the parvalbumin-positive cells closely resembled the knotty type 2 amacrine cells described using the Golgi method in macaques. They contained immunoreactive glycine transporter, but not immunoreactive γ-aminobutyric acid, and therefore, they use glycine as their neurotransmitter. Their spatial density was relatively high, roughly half that of AII amacrine cells. They contacted lobular dendrites of AII cells, and they are expected to be presynaptic to AII cells based on earlier ultrastructural studies. They also made extensive contacts with axon terminals of OFF midget bipolar cells whose polarity cannot be predicted with certainty. A macaque amacrine cell of the same morphological type depolarized at the onset of increments in light intensity, and it was well coupled to other amacrine cells. Previously, we described amacrine cells like these that contacted OFF parasol ganglion cells and OFF starburst amacrine cells. Taken together, these findings suggest that one function of these amacrine cells is to inhibit the transmission of signals from rods to OFF bipolar cells via AII amacrine cells. Another function may be inhibition of the OFF pathway following increments in light intensity.


2001 ◽  
Vol 437 (4) ◽  
pp. 408-422 ◽  
Author(s):  
E. Brady Trexler ◽  
Wei Li ◽  
Stephen L. Mills ◽  
Stephen C. Massey

2016 ◽  
Vol 115 (1) ◽  
pp. 389-403 ◽  
Author(s):  
Yifan Zhou ◽  
Barbora Tencerová ◽  
Espen Hartveit ◽  
Margaret L. Veruki

At many glutamatergic synapses, non- N-methyl-d-aspartate (NMDA) and NMDA receptors are coexpressed postsynaptically. In the mammalian retina, glutamatergic rod bipolar cells are presynaptic to two rod amacrine cells (AII and A17) that constitute dyad postsynaptic partners opposite each presynaptic active zone. Whereas there is strong evidence for expression of non-NMDA receptors by both AII and A17 amacrines, the expression of NMDA receptors by the pre- and postsynaptic neurons in this microcircuit has not been resolved. In this study, using patch-clamp recording from visually identified cells in rat retinal slices, we investigated the expression and functional properties of NMDA receptors in these cells with a combination of pharmacological and biophysical methods. Pressure application of NMDA did not evoke a response in rod bipolar cells, but for both AII and A17 amacrines, NMDA evoked responses that were blocked by a competitive antagonist (CPP) applied extracellularly and an open channel blocker (MK-801) applied intracellularly. NMDA-evoked responses also displayed strong Mg2+-dependent voltage block and were independent of gap junction coupling. With low-frequency application (60-s intervals), NMDA-evoked responses remained stable for up to 50 min, but with higher-frequency stimulation (10- to 20-s intervals), NMDA responses were strongly and reversibly suppressed. We observed strong potentiation when NMDA was applied in nominally Ca2+-free extracellular solution, potentially reflecting Ca2+-dependent NMDA receptor inactivation. These results indicate that expression of functional (i.e., conductance-increasing) NMDA receptors is common to both AII and A17 amacrine cells and suggest that these receptors could play an important role for synaptic signaling, integration, or plasticity in the rod pathway.


1982 ◽  
Vol 47 (5) ◽  
pp. 928-947 ◽  
Author(s):  
R. Nelson

1. In a perfused eyecup preparation, AII amacrine cells of the cat retina were penetrated with glass microelectrodes and their electrical responses to photic stimuli recorded. 2. Intracellular injections of the stains Procion, lucifer, or horseradish peroxidase revealed dendritic tree diameters of 30-80 micrometers (48 +/- 16 micrometers, mean +/0 SD) and cell body diameters from 7 to 12 micrometers (9 +/- 3 micrometers) for these cells. The dendrites were broadly stratified throughout the inner plexiform layer (IPL) but possessed large, terminal varicosities in the IPL and inner nuclear lyer (INL) proximal to the cell body. 3. The waveform of these cells in response to photic stimulation suggested division into four components: a) an initial rapid depolarization of the cell membrane followed by a slower decay toward the dark level; b) suppression of the dark noise of the cell; c) with dim or moderately intense stimuli, an off-hyperpolarization; d) in some cases a hyperpolarizing surround response. 4. The receptive fields of AII cells have been characterized using spatial stimuli consisting of long narrow slits. Curves have been fitted to spatial data using two space constants, one for the center mechanism and an opposing one for the surround. For the central mechanism, space constants ranged from 20 to 80 micrometers (46 +/- 22 micrometers), while for the surround they ranged from 60 to 130 micrometers (85 +/- 28 micrometers). The mean half-width of the center mechanism, calculated from the mean space constant, was about 0.25 degrees of visual angle (64 micrometers). The receptive-field properties of AII amacrine cells resemble those of center-depolarizing bipolar cells of other species. 5. Spectral studies of AII amacrine cells reveal that they are rod driven at all criterion voltage levels. Furthermore, adaptation of the rods by rod-saturating backgrounds eliminates 95% of the response amplitude of the AII amacrine cells. Under these conditions the tiny response component remaining is driven by the cat's long wavelength (556-nm peak) cones. 6. AII amacrine cells depolarize to rod stimulation more rapidly than other rod-dominated cells, such as rod bipolar cells, which hyperpolarize. For stimuli corresponding to about 10% of rod saturation, the latency to half-maximum amplitude is about 65 ms for AII cells, 40 ms faster than rod-dominated hyperpolarizing units. The leading edge of the response waveform for AII cells is also much more restricted in time. With the above stimulus it requires about 20 ms to increase from 25 to 75% of its peak, a period almost 4 times shorter than required by rod-dominated S-potential responses. With saturating stimuli the AII response requires only 5 ms to increase from 25 ot 75% of its peak. 7. Although prominent in the rod system, AII amacrine cells do not appear to be able to detect single quantum events. Threshold signals require the bleaching of about 200 rhodopsin molecules within a receptive field containing some 1,300 rods...


1999 ◽  
Vol 16 (6) ◽  
pp. 1105-1114 ◽  
Author(s):  
PU QIN ◽  
ROBERTA G. POURCHO

AMPA-selective glutamate receptors play a major role in glutamatergic neurotransmission in the retina and are expressed in a variety of neuronal subpopulations. In the present study, immunocytochemical techniques were used to visualize the distribution of GluR2 and GluR4 subunits in the cat retina. Results were compared with previous localizations of GluR1 and GluR2/3. Staining for GluR2 was limited to a small number of amacrine and ganglion cells whereas GluR4 staining was present in A-type horizontal cells, many amacrine cells including type AII amacrine cells, and the majority of the cells in the ganglion cell layer. Analysis of synaptic relationships in the outer plexiform layer showed the GluR4 subunit to be concentrated at the contacts of cone photoreceptors with A-horizontal cells. In the inner plexiform layer, both GluR2 and GluR4 were postsynaptic to cone bipolar cells at dyad contacts although GluR2 staining was limited to one of the postsynaptic elements whereas GluR4 immunoreactivity was often seen in both postsynaptic elements. Unlike GluR2, GluR4 was also postsynaptic to rod bipolar cells where it could be visualized in processes of AII amacrine cells. The data indicate that GluR3 and GluR4 subunits are colocalized in a number of cell types including A-type horizontal cells, AII amacrine cells, and alpha ganglion cells, but whether they are combined in the same multimeric receptors remains to be determined.


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