Synaptic microcircuitry of bipolar and amacrine cells with serotonin-like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans

1993 ◽  
Vol 10 (3) ◽  
pp. 455-471 ◽  
Author(s):  
Lawrence B. Hurd ◽  
William D. Eldred
Keyword(s):  
Bipolar Cell ◽  
Amacrine Cell ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Outer Plexiform Layer ◽  
Inner Plexiform Layer ◽  
Synaptic Contacts ◽  
Synaptic Inputs ◽  
Cell Processes

AbstractAlthough serotonin is thought to be a neurotransmitter in a number of retinal systems, much of the precise synaptic connectivity of serotonergic neurons is unknown. To address this issue, we used an antiserum directed against serotonin to label serotonergic bipolar and amacrine cells in the turtle retina. Light-microscopic analysis of labeled amacrine and bipolar cells indicated that both had bistratified dendritic arborizations primarily in stratum 1 and in strata 4/5 of the inner plexiform layer.Ultrastructural analysis of the neurocircuitry of these cells indicated that the processes of labeled bipolar cells in the outer plexiform layer made basal junction contacts with photoreceptor terminals. Only in rare instances did labeled bipolar cells processes invaginate near photoreceptor ribbon synapses. Processes of labeled bipolar cells received both conventional and small ribbon synaptic contacts in the outer plexiform layer. Bipolar cell processes in stratum 1 of the inner plexiform layer synapsed onto either amacrine/amacrine or amacrine/ganglion cell dyads, and made rare ribbon synaptic contacts onto labeled amacrine cell processes. Synaptic inputs to serotonergic bipolar cells in stratum 1 were from unlabeled bipolar and amacrine cells. Bipolar cell contacts in strata 4/5 were similar to those in stratum 1, but were fewer in number and no bipolar cell inputs were seen.Labeled amacrine cell output in both strata was onto other unlabeled amacrine cells and ganglion cells; but synaptic outputs to unlabeled bipolar cells were only seen in strata 4/5. In both strata 1 and 4/5, synaptic inputs to labeled amacrine cells were from both unlabeled amacrine cells and labeled bipolar cells. The serotonergic amacrine cells had many more synaptic interactions in stratum 1 than in strata 4/5 which supports the role of serotonergic bipolar cells in the OFF pathway of retinal processing. Interactions between serotonergic bipolar and amacrine cells may play an important role in visual processing.

Synaptic circuitry of neuropeptide-containing amacrine cells in the retina of the cane toad, Bufo marinus

1995 ◽  
Vol 12 (5) ◽  
pp. 919-927 ◽  
Author(s):  
Bao-Song Zhu ◽  
Ian Gibbins
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bufo Marinus ◽  
Inner Plexiform Layer ◽  
Cane Toad ◽  
Synaptic Inputs ◽  
Cell Processes

AbstractSynaptic connections of amacrine cells with substance P-like or neuropeptide Y-like immunoreactivity (SP-LI or NPY-LI) in the retina of the cane toad, Bufo marinus, were investigated using ultrastructural immunocytochemistry. The perikarya of SP-LI or NPY-LI amacrine cells were located in the innermost row of the inner nuclear layer. The synapses associated with SP-LI amacrine cells were distributed mainly in sublaminae 3 and 4 with about 10% in sublamina 1 of the inner plexiform layer. The synapses formed by NPY-LI amacrine cells were found in sublaminae 1, 2, and 4 with approximately equal frequency. Of a total of 175 SP-LI profiles, 56% were in presynaptic positions and 44% in postsynaptic positions. The synaptic inputs to SP-LI profiles predominantly derived from other unlabeled amacrine cell dendrites, and to a lesser extent, from bipolar cell terminals. The majority of synaptic outputs from SP-LI amacrine cell dendrites were directed onto unlabeled amacrine cell processes. The SP-LI profiles also made synapses onto bipolar cell terminals and formed synapses onto presumed ganglion cell dendrites. Of a total of 200 NPY-LI profiles, 48% were in presynaptic positions and 52% in postsynaptic positions. The profiles of NPY-LI amacrine cells mainly received their synaptic inputs from other unlabeled amacrine cell processes, and to a lesser extent, from bipolar cell terminals. The majority of NPY-LI amacrine cell profiles gave their synaptic outputs onto unlabeled amacrine cell dendrites, and others formed synapses onto presumed ganglion cell processes. These results suggest that these two populations of neuropeptide-containing amacrine cells in the Bufo retina are involved in different synaptic circuits.

scholarly journals Synaptic input to an ON parasol ganglion cell in the macaque retina: A serial section analysis

2002 ◽  
Vol 19 (3) ◽  
pp. 299-305 ◽  
Author(s):  
DAVID W. MARSHAK ◽  
ELIZABETH S. YAMADA ◽  
ANDREA S. BORDT ◽  
WENDY C. PERRYMAN
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inhibitory Input ◽  
Inner Plexiform Layer ◽  
Cell Processes

A labeled ON parasol ganglion cell from a macaque retina was analyzed in serial, ultrathin sections. It received 13% of its input from diffuse bipolar cells. These directed a large proportion of their output to amacrine cells but received a relatively small proportion of their amacrine cell input via feedback synapses. In these respects, they were similar to the DB3 bipolar cells that make synapses onto OFF parasol cells. Bipolar cell axons that contacted the ON parasol cell in stratum 4 of the inner plexiform layer always made synapses onto the dendrite, and therefore, the number of bipolar cell synapses onto these ganglion cells could be estimated reliably by light microscopy in the future. Amacrine cells provided the majority of inputs to the ON parasol cell. Only a few of the presynaptic amacrine cell processes received inputs from the same bipolar cells as the parasol cells, and most of the presynaptic amacrine cell processes did not receive any inputs at all within the series. These findings suggest that most of the inhibitory input to the ON parasol cell originates from other areas of the retina. Amacrine cells presynaptic to the parasol ganglion cell interacted very infrequently with other neurons in the circuit, and therefore, they would be expected to act independently, for the most part.

scholarly journals Heterocellular coupling between amacrine cell and ganglion cells

2018 ◽  
Author(s):  
Robert E. Marc ◽  
Crystal Sigulinsky ◽  
Rebecca L. Pfeiffer ◽  
Daniel Emrich ◽  
James R. Anderson ◽  
...  
Keyword(s):  
Gap Junctions ◽  
Ganglion Cell ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Tem Analysis

AbstractAll superclasses of retinal neurons display some form of electrical coupling including the key neurons of the inner plexiform layer: bipolar cells (BCs), amacrine or axonal cells (ACs) and ganglion cells (GCs). However, coupling varies extensively by class. For example, mammalian rod bipolar cells form no gap junctions at all, while all cone bipolar cells form class-specific coupling arrays, many of them homocellular in-superclass arrays. Ganglion cells are unique in that classes with coupling predominantly form heterocellular cross-class arrays of ganglion cell::amacrine cell (GC::AC) coupling in the mammalian retina. Ganglion cells are the least frequent superclass in the inner plexiform layer and GC::AC gap junctions are sparsely arrayed amidst massive cohorts of AC::AC, bipolar cell BC::BC, and AC::BC gap junctions. Many of these gap junctions and most ganglion cell gap junctions are suboptical, complicating analysis of specific ganglion cells. High resolution 2 nm TEM analysis of rabbit retinal connectome RC1 allows quantitative GC::AC coupling maps of identified ganglion cells. Ganglion cells classes apparently avoid direct cross-class homocellular coupling altogether even though they have opportunities via direct membrane touches, while transient OFF alpha ganglion cells and transient ON directionally selective (DS) ganglion cells are strongly coupled to distinct amacrine / axonal cell cohorts.A key feature of coupled ganglion cells is intercellular metabolite flux. Most GC::AC coupling involves GABAergic cells (γ+ amacrine cells), which results in significant GABA flux into ganglion cells. Surveying GABA coupling signatures in the ganglion cell layer across species suggests that the majority of vertebrate retinas engage in GC::AC coupling.Multi-hop synaptic queries of the entire RC1 connectome clearly profiles the coupled amacrine and axonal cells. Photic drive polarities and source bipolar cell class selec-tivities are tightly matched across coupled cells. OFF alpha ganglion cells are coupled to OFF γ+ amacrine cells and transient ON DS ganglion cells are coupled to ON γ+ amacrine cells including a large interstitial axonal cell (IAC). Synaptic tabulations show close matches between the classes of bipolar cells sampled by the coupled amacrine and ganglion cells. Further, both ON and OFF coupling ganglion networks show a common theme: synaptic asymmetry whereby the coupled γ+ neurons are also presynaptic to ganglion cell dendrites from different classes of ganglion cells outside the coupled set. In effect, these heterocellular coupling patterns enable an excited ganglion cell to directly inhibit nearby ganglion cells of different classes. Similarly, coupled γ+ amacrine cells engaged in feedback networks can leverage the additional gain of bipolar cell synapses in shaping the signaling of a spectrum of downstream targets based on their own selective coupling with ganglion cells.

Organization of the primate retina: electron microscopy

1966 ◽  
Vol 166 (1002) ◽  
pp. 80-111 ◽  
Keyword(s):  
Electron Microscopy ◽  
Ganglion Cell ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Receptor Cell ◽  
Plexiform Layer ◽  
Cell Physiology ◽  
Inner Plexiform Layer ◽  
Synaptic Contacts ◽  
Cell Processes

The retinae of monkey and man have been studied by electron microscopy to identify cell types, their processes and synaptic contacts. In the inner plexiform layer, the morphological characteristics of the three types of cells (bipolar, ganglion and amacrine) are described and seven synaptic relationships are identified. The bipolar terminals contain ribbons at points of synaptic contact, and, at these points, there are typically two postsynaptic processes, one a ganglion cell dendrite, the other an amacrine cell process. This synaptic arrangement is here termed a dyad. The amacrine cell processes themselves make synaptic contacts with ganglion cell dendrites and somata, other amacrine cell processes, and, most frequently, with the bipolar cell terminals. Often, the amacrine-bipolar contact is adjacent to a bipolar-amacrine junction, forming a reciprocal synaptic arrangement between the bipolar and the amacrine. In the more peripheral retina, large bipolar cell terminals (probably of rod bipolars) are occasionally observed adjacent to the perikarya of the ganglion cells. At these junctions, areas of fusion between the plasma membranes are seen, suggesting that such axosomatic junctions could be electrical. In the outer plexiform layer, synapses have been identified only in the receptor cell bases where receptor cells contact bipolar and horizontal cell processes. Synaptic contacts of the horizontal cells have not been clearly identified, but their strategic terminations in the receptor cell ending are described and interpreted as possibly synaptic. A model of the retina, based on the described anatomy, is presented and correlated with ganglion cell physiology.

Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates

1968 ◽  
Vol 170 (1019) ◽  
pp. 205-228 ◽  
Keyword(s):  
Synaptic Vesicles ◽  
Synaptic Contact ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Outer Plexiform Layer ◽  
Inner Plexiform Layer ◽  
Synaptic Organization ◽  
Synaptic Contacts ◽  
Frog Retina ◽  
Cell Processes

The synaptic contacts in the inner and outer plexiform layers of the frog retina have been identified and studied by electron microscopy. In the inner plexiform layer, two types of synaptic contact were recognized. One type, believed to be the synaptic contact of the bipolar terminals, is characterized by a synaptic ribbon in the presynaptic cytoplasm. At such ribbon contacts, there are ordinarily two postsynaptic elements, both of which usually contain numerous synaptic vesicles and appear morphologically identical. The second type of synaptic contact in the inner plexiform layer has a more conventional morpho­logy and is observed very much more frequently than are the ribbon contacts. It is characterized by a dense aggregation of synaptic vesicles clustered close to the presynaptic membrane and is thought to be the synaptic contact of the amacrine processes. The conventional synapses are presynaptic to ribbon-containing processes, ganglion cell dendrites, and other amacrine cell processes. Reciprocal contacts between processes making ribbon synapses, and processes making conventional synapses are often observed. Serial synapses between morphologically identical processes, presumably amacrine processes, are frequently seen; and up to four synapses in series between five adjacent processes have been observed. These findings suggest that in the inner plexiform layer of the frog: (1) bipolar terminals synapse primarily with amacrine processes; (2) amacrine processes synapse extensively with the processes of other amacrine cells; and (3) ganglion cells are driven primarily by the amacrine cells. In the outer plexiform layer, processes penetrate into invaginations in the bases of the receptor terminals and lie in close proximity to the synaptic ribbons of the terminals, where the processes presumably receive synaptic input from the receptors. Elsewhere in the outer plexiform layer, knob-like processes, probably from horizontal cells, make conventional synaptic contacts with other horizontal cell processes and probably with bipolar dendrites.

Disruption of transient photoreceptor targeting within the inner plexiform layer following early ablation of cholinergic amacrine cells in the ferret

2001 ◽  
Vol 18 (5) ◽  
pp. 741-751 ◽  
Author(s):  
P.T. JOHNSON ◽  
M.A. RAVEN ◽  
B.E. REESE
Keyword(s):  
Retinal Ganglion Cells ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Inner Plexiform Layer ◽  
Retinal Ganglion ◽  
Subcutaneous Injections ◽  
Cell Processes ◽  
Cholinergic Amacrine Cells

Photoreceptors in the ferret's retina have been shown to project transiently to the inner plexiform layer (IPL) prior to their differentiation of an outer segment. On postnatal day 15 (P-15), when this projection achieves maximal density, the photoreceptors projecting into the IPL extend primarily to one of two depths, coincident with the processes of cholinergic amacrine cells. The present study has used an excitotoxic approach employing subcutaneous injections of l-glutamate to ablate these cholinergic amacrine cells on P-7, in order to see whether their elimination alters this targeting of photoreceptor terminals within the IPL. The near-complete elimination of cholinergic amacrine cells at P-15 was confirmed, although the population of retinal ganglion cells was also affected, being depleted by roughly 50%. The rod opsin-immunopositive terminals in such treated ferrets no longer showed a stratified distribution, being found throughout the depth of the IPL, as well as extending into the ganglion cell layer. This effect should not be due to the partial loss of retinal ganglion cells, however, since optic nerve transection at P-2, which eliminates the ganglion cells entirely while leaving the cholinergic amacrine cell population intact, was shown not to affect the stratification pattern of the photoreceptors within the IPL. These results strongly suggest that the targeting of the photoreceptor terminals to discrete strata within the IPL is dependent upon the cholinergic amacrine cell processes.

scholarly journals Analysis of synaptic inputs to on-off amacrine cells of the carp retina.

1988 ◽  
Vol 92 (4) ◽  
pp. 475-487 ◽  
Author(s):  
T Kujiraoka ◽  
T Saito ◽  
J Toyoda
Keyword(s):  
Cell Membrane ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Evoked Responses ◽  
Intracellular Recordings ◽  
Current Step ◽  
Synaptic Inputs ◽  
Synaptic Process

To elucidate the synaptic transmission between bipolar cells and amacrine cells, the effect of polarization of a bipolar cell on an amacrine cell was examined by simultaneous intracellular recordings from both cells in the isolated carp retina. When either an ON or OFF bipolar cell was depolarized by an extrinsic current step, an ON-OFF amacrine cell was transiently depolarized at the onset of the current but no sustained polarization during the current was detected. The current hyperpolarizing the OFF bipolar cell also produced the transient depolarization of the amacrine cell at the termination of the current. These responses had a latency of approximately 10 ms. The amplitude of the current-evoked responses changed gradually with current intensity within the range used in these experiments. They were affected by polarization of the amacrine cell membrane; the amplitude of the current-evoked responses as well as the light-evoked responses was increased when the amacrine cell membrane was hyperpolarized, while the amplitude was decreased when the cell was depolarized. These results confirm directly that ON-OFF amacrine cells receive excitatory inputs from both ON and OFF bipolar cells: the ON transient is due to inputs from ON bipolar cells, and the OFF transient to inputs from OFF bipolar cells. The steady polarization of bipolar cells is converted into transient signals during the synaptic process.

The photoresponses of structurally identified amacrine cells in the turtle retina

1982 ◽  
Vol 214 (1196) ◽  
pp. 403-415 ◽  
Keyword(s):  
Time Course ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Homogeneous Distribution ◽  
Inner Plexiform Layer ◽  
Intracellular Recordings ◽  
Cell Processes ◽  
Layer I

Intracellular recordings were obtained from amacrine cells afterwards identified morphologically by horseradish peroxidase injection. There is a correlation between the time course of the photoresponses and the distribution of the cell processes across the inner plexiform layer (i. p. l.). Cells producing the shortest duration, transient ‘on‒off’ photoresponses branched in a single, narrow stratum of the i. p. l. (3‒7 μm across). Transient photoresponses with a longer time course were recorded from cells branching in a thicker stratum of i. p. l. (up to 20 μm), or from bistratified cells. Amacrine cells producing sustained centre-on or centre-off photoresponses were radially diffused across the whole i. p. l.; therefore this type of photoresponse need not be associated with a specific cellular stratification within the i. p. l. It is concluded that the two main functional types of amacrine cell, i. e. transient on‒off and sustained centre-on and centre-off, are subject to different structural organization of inputs than are the homologous physiological types of ganglion cells in this species, in the cat and in the carp. In a summary diagram the observed characteristics of the photoresponses are tentatively explained in term s of a non-homogeneous distribution of bipolar synaptic inputs along amacrine cell processes.

scholarly journals Differential encoding of spatial information among retinal on cone bipolar cells

2015 ◽  
Vol 114 (3) ◽  
pp. 1757-1772 ◽  
Author(s):  
Robert J. Purgert ◽  
Peter D. Lukasiewicz
Keyword(s):  
Parallel Processing ◽  
Visual Processing ◽  
Amacrine Cell ◽  
Spatial Information ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Spatial Tuning ◽  
Cone Bipolar Cells

The retina is the first stage of visual processing. It encodes elemental features of visual scenes. Distinct cone bipolar cells provide the substrate for this to occur. They encode visual information, such as color and luminance, a principle known as parallel processing. Few studies have directly examined whether different forms of spatial information are processed in parallel among cone bipolar cells. To address this issue, we examined the spatial information encoded by mouse ON cone bipolar cells, the subpopulation excited by increments in illumination. Two types of spatial processing were identified. We found that ON cone bipolar cells with axons ramifying in the central inner plexiform layer were tuned to preferentially encode small stimuli. By contrast, ON cone bipolar cells with axons ramifying in the proximal inner plexiform layer, nearest the ganglion cell layer, were tuned to encode both small and large stimuli. This dichotomy in spatial tuning is attributable to amacrine cells providing stronger inhibition to central ON cone bipolar cells compared with proximal ON cone bipolar cells. Furthermore, background illumination altered this difference in spatial tuning. It became less pronounced in bright light, as amacrine cell-driven inhibition became pervasive among all ON cone bipolar cells. These results suggest that differential amacrine cell input determined the distinct spatial encoding properties among ON cone bipolar cells. These findings enhance the known parallel processing capacity of the retina.

Synaptic organization of GABAergic amacrine cells in the salamander retina

2004 ◽  
Vol 21 (6) ◽  
pp. 817-825 ◽  
Author(s):  
JUN ZHANG ◽  
HO-HWA WANG ◽  
CHEN-YU YANG
Keyword(s):  
Amacrine Cell ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Synaptic Organization ◽  
Proximal Margin ◽  
Functional Roles ◽  
Small Peak ◽  
Immuno Electron Microscopy

The synaptic organization of GABA-immunoreactive (GABA-IR) amacrine cells in the inner plexiform layer (IPL) of salamander retina was studied with the use of postembedding immuno-electron microscopy. A total of 457 GABA-IR amacrine synapses, with identified postsynaptic elements, were analyzed on photomontages of electron micrographs covering 3,618 μm2 of the IPL. GABA-IR amacrine synapses were distributed throughout the IPL, with a small peak at the proximal margin of sublamina a. The majority of the output targets (81%) were GABA(−) neurons. Most of the contacts were simple synapses with one postsynaptic element identified as a process of an amacrine cell (55%), bipolar cell (19%) or ganglion cell (26%), and serial synapses were very rare. Of the 89 postsynaptic bipolar terminals, 63% participated in a reciprocal feedback synapse with the same presynaptic GABA-IR amacrine profile. There appeared to be no preference between GABA-IR amacrine contacts with rod- or cone-dominated bipolar cells (9.1% vs. 8.9%) or in the total number of amacrine synapses in sublaminas a and b (52% vs. 47%). The preponderance of amacrine cell input to bipolar cells in the OFF layer was derived from GABA-IR cells. These findings provide ultrastructural support to the existing physiological studies regarding the functional roles of the GABAergic amacrine cells in this species. Our results have added to the data base demonstrating that, in contrast to mammals, GABA-IR amacrine cells in amphibians and other nonmammals contact other amacrine cells more frequently, suggesting greater involvement of GABAergic amacrine cells in modulating lateral inhibitory pathways.

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