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Dynamic Range of Vertebrate Retina Ganglion Cells: Importance of Active Dendrites and Coupling by Electrical Synapses
Rodrigo Publio,Cesar Celis Ceballos,Antonio C. Roque
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0048517
Abstract: The vertebrate retina has a very high dynamic range. This is due to the concerted action of its diverse cell types. Ganglion cells, which are the output cells of the retina, have to preserve this high dynamic range to convey it to higher brain areas. Experimental evidence shows that the firing response of ganglion cells is strongly correlated with their total dendritic area and only weakly correlated with their dendritic branching complexity. On the other hand, theoretical studies with simple neuron models claim that active and large dendritic trees enhance the dynamic range of single neurons. Theoretical models also claim that electrical coupling between ganglion cells via gap junctions enhances their collective dynamic range. In this work we use morphologically reconstructed multi-compartmental ganglion cell models to perform two studies. In the first study we investigate the relationship between single ganglion cell dynamic range and number of dendritic branches/total dendritic area for both active and passive dendrites. Our results support the claim that large and active dendrites enhance the dynamic range of a single ganglion cell and show that total dendritic area has stronger correlation with dynamic range than with number of dendritic branches. In the second study we investigate the dynamic range of a square array of ganglion cells with passive or active dendritic trees coupled with each other via dendrodendritic gap junctions. Our results suggest that electrical coupling between active dendritic trees enhances the dynamic range of the ganglion cell array in comparison with both the uncoupled case and the coupled case with cells with passive dendrites. The results from our detailed computational modeling studies suggest that the key properties of the ganglion cells that endow them with a large dynamic range are large and active dendritic trees and electrical coupling via gap junctions.
Spatial Relationships between GABAergic and Glutamatergic Synapses on the Dendrites of Distinct Types of Mouse Retinal Ganglion Cells across Development  [PDF]
Adam Bleckert, Edward D. Parker, YunHee Kang, Raika Pancaroglu, Florentina Soto, Renate Lewis, Ann Marie Craig, Rachel O. L. Wong
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0069612
Abstract: Neuronal output requires a concerted balance between excitatory and inhibitory (I/E) input. Like other circuits, inhibitory synaptogenesis in the retina precedes excitatory synaptogenesis. How then do neurons attain their mature balance of I/E ratios despite temporal offset in synaptogenesis? To directly compare the development of glutamatergic and GABAergic synapses onto the same cell, we biolistically transfected retinal ganglion cells (RGCs) with PSD95CFP, a marker of glutamatergic postsynaptic sites, in transgenic Thy1-YFPγ2 mice in which GABAA receptors are fluorescently tagged. We mapped YFPγ2 and PSD95CFP puncta distributions on three RGC types at postnatal day P12, shortly before eye opening, and at P21 when robust light responses in RGCs are present. The mature IGABA/E ratios varied among ON-Sustained (S) A-type, OFF-S A-type, and bistratified direction selective (DS) RGCs. These ratios were attained at different rates, before eye-opening for ON-S and OFF-S A-type, and after eye-opening for DS RGCs. At both ages examined, the IGABA/E ratio was uniform across the arbors of the three RGC types. Furthermore, measurements of the distances between neighboring PSD95CFP and YFPγ2 puncta on RGC dendrites indicate that their local relationship is established early in development, and cannot be predicted by random organization. These close spatial associations between glutamatergic and GABAergic postsynaptic sites appear to represent local synaptic arrangements revealed by correlative light and EM reconstructions of a single RGC's dendrites. Thus, although RGC types have different IGABA/E ratios and establish these ratios at separate rates, the local relationship between excitatory and inhibitory inputs appear similarly constrained across the RGC types studied.
Developmental patterning of glutamatergic synapses onto retinal ganglion cells
Josh L Morgan, Timm Schubert, Rachel OL Wong
Neural Development , 2008, DOI: 10.1186/1749-8104-3-8
Abstract: We transfected developing and mature mouse RGCs with plasmids encoding fluorescent proteins that label their dendrites and glutamatergic postsynaptic sites. We found that as dendritic density (dendritic length per unit area of dendritic field) decreases with maturation, the density of synapses along the dendrites increases. These changes appear coordinated such that RGCs attain the mature average density of postsynaptic sites per unit area (areal density) by the time synaptic function emerges. Furthermore, stereotypic centro-peripheral gradients in the areal density of synapses across the arbor of RGCs are established at an early developmental stage.The spatial pattern of glutamatergic inputs onto RGCs arises early in synaptogenesis despite ensuing reorganization of dendritic structure. We raise the possibility that these early patterns of synaptic distributions may arise from constraints placed on the number of contacts presynaptic neurons are able to make with the RGCs.Glutamatergic inputs provide the major excitatory drive onto neurons in the central nervous system (CNS). Much is known about how individual glutamatergic synapses are formed, maintained or eliminated during development [1-3]. The physiological function of postsynaptic cells, however, does not depend solely on how individual synapses are assembled. It also depends on the how the correct number, density, and often spatial distribution of these synapses are established across the dendritic arbor. How distinct spatial patterns of glutamatergic synaptic inputs are established during development is poorly understood. Addressing this fundamental issue appears more tractable in the retina than elsewhere in the CNS, largely because the functional input/output characteristics of its neurons have been well characterized and correlated with cellular morphology and circuitry [4].In the vertebrate retina, many of the functional properties of retinal ganglion cells (RGCs) are determined by the lateral and vertica
Axonal Synapses Utilize Multiple Synaptic Ribbons in the Mammalian Retina  [PDF]
Hong-Lim Kim, Ji Hyun Jeon, Tae-Hyung Koo, U-Young Lee, Eojin Jeong, Myung-Hoon Chun, Jung-Il Moon, Stephen C. Massey, In-Beom Kim
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0052295
Abstract: In the mammalian retina, bipolar cells and ganglion cells which stratify in sublamina a of the inner plexiform layer (IPL) show OFF responses to light stimuli while those that stratify in sublamina b show ON responses. This functional relationship between anatomy and physiology is a key principle of retinal organization. However, there are at least three types of retinal neurons, including intrinsically photosensitive retinal ganglion cells (ipRGCs) and dopaminergic amacrine cells, which violate this principle. These cell types have light-driven ON responses, but their dendrites mainly stratify in sublamina a of the IPL, the OFF sublayer. Recent anatomical studies suggested that certain ON cone bipolar cells make axonal or ectopic synapses as they descend through sublamina a, thus providing ON input to cells which stratify in the OFF sublayer. Using immunoelectron microscopy with 3-dimensional reconstruction, we have identified axonal synapses of ON cone bipolar cells in the rabbit retina. Ten calbindin ON cone bipolar axons made en passant ribbon synapses onto amacrine or ganglion dendrites in sublamina a of the IPL. Compared to the ribbon synapses made by bipolar terminals, these axonal ribbon synapses were characterized by a broad postsynaptic element that appeared as a monad and by the presence of multiple short synaptic ribbons. These findings confirm that certain ON cone bipolar cells can provide ON input to amacrine and ganglion cells whose dendrites stratify in the OFF sublayer via axonal synapses. The monadic synapse with multiple ribbons may be a diagnostic feature of the ON cone bipolar axonal synapse in sublamina a. The presence of multiple ribbons and a broad postsynaptic density suggest these structures may be very efficient synapses. We also identified axonal inputs to ipRGCs with the architecture described above.
Coordinated increase in inhibitory and excitatory synapses onto retinal ganglion cells during development
Florentina Soto, Adam Bleckert, Renate Lewis, Yunhee Kang, Daniel Kerschensteiner, Ann Marie Craig, Rachel OL Wong
Neural Development , 2011, DOI: 10.1186/1749-8104-6-31
Abstract: We demonstrate that YFP-NL2 is present at inhibitory synapses in the inner plexiform layer by its co-localization with gephyrin, the γ2 subunit of the GABAA receptor and glycine receptors. YFP-NL2 puncta were apposed to the vesicular inhibitory transmitter transporter VGAT but not to CtBP2, a marker of presynaptic ribbons found at bipolar cell terminals. Similar patterns of co-localization with synaptic markers were observed for endogenous NL2. We also verified that expression of YFP-NL2 in the transgenic line did not significantly alter spontaneous inhibitory synaptic transmission onto RGCs. Using these mice, we found that, on average, the density of inhibitory synapses on individual arbors increased gradually until eye opening (postnatal day 15). A small centro-peripheral gradient in density found in mature arbors was apparent at the earliest age we examined (postnatal day 8). Unexpectedly, the adult ratio of inhibitory/excitatory postsynaptic sites was rapidly attained, shortly after glutamatergic synaptogenesis commenced (postnatal day 7).Our observations suggest that bipolar and amacrine cell synaptogenesis onto RGCs appear coordinated to rapidly attain a balanced ratio of excitatory and inhibitory synapse densities prior to the onset of visual experience.The normal functioning of the nervous system requires balanced excitatory and inhibitory neurotransmission. If excitation or inhibition is perturbed, neurons undergo alterations in their intrinsic excitability and synaptic transmission in order to restore a balance, and prevent their circuits from undergoing epileptiform activity [1,2]. While such homeostatic plasticity in mature neuronal networks is well studied [3], much less is known concerning how balanced excitation and inhibition is normally achieved during development. In many parts of the central nervous system (CNS), interneurons containing the classical inhibitory transmitters γ-aminobutyric acid (GABA) or glycine form functional synaptic connections
Ultrastructural characterization of GABAergic and excitatory synapses in the inferior colliculus  [PDF]
Kyle T. Nakamoto,Jeffrey G. Mellott,Colleen S. Sowick,Brett R. Schofield
Frontiers in Neuroanatomy , 2014, DOI: 10.3389/fnana.2014.00108
Abstract: In the inferior colliculus (IC) cells integrate inhibitory input from the brainstem and excitatory input from both the brainstem and auditory cortex. In order to understand how these inputs are integrated by IC cells identification of their synaptic arrangements is required. We used electron microscopy to characterize GABAergic synapses in the dorsal cortex, central nucleus, and lateral cortex of the IC (ICd, ICc, and IClc) of guinea pigs. Throughout the IC, GABAergic synapses are characterized by pleomorphic vesicles and symmetric junctions. Comparisons of GABAergic synapses with excitatory synapses revealed differences (in some IC subdivisions) between the distributions of these synapse types onto IC cells. For excitatory cells in the IClc and ICd GABAergic synapses are biased toward the somas and large dendrites, whereas the excitatory boutons are biased toward spines and small dendrites. This arrangement could allow for strong inhibitory gating of excitatory inputs. Such differences in synaptic distributions were not observed in the ICc, where the two classes of bouton have similar distributions along the dendrites of excitatory cells. Interactions between excitatory and GABAergic inputs on the dendrites of excitatory ICc cells may be more restricted (i.e., reflecting local dendritic processing) than in the other IC subdivisions. Comparisons across IC subdivisions revealed evidence for two classes of GABAergic boutons, a small GABAergic (SG) class that is present throughout the IC and a large GABAergic (LG) class that is almost completely restricted to the ICc. In the ICc, LG, and SG boutons differ in their targets. SG boutons contact excitatory dendritic shafts most often, but also contact excitatory spines and somas (excitatory and GABAergic). LG synapses make comparatively fewer contacts on excitatory shafts, and make comparatively more contacts on excitatory spines and on somas (excitatory and GABAergic). LG boutons likely have a lemniscal origin.
Xenopus laevis Retinal Ganglion Cell Dendritic Arbors Develop Independently of Visual Stimulation  [PDF]
Rebecca L. Rigel,Barbara Lom
Impulse : an Undergraduate Journal for Neuroscience , 2004,
Abstract: Newly formed neurons must locate their appropriate target cells and then form synaptic connections with these targets in order to establish a functional nervous system. In the vertebrate retina, retinal ganglion cell (RGC) dendrites extend from the cell body and form synapses with nearby amacrine and bipolar cells. RGC axons, however, exit the retina and synapse with the dendrites of midbrain neurons in the optic tectum. We examined how visual stimulation influenced Xenopus RGC dendritic arborization. Neuronal activity is known to be an important factor in shaping dendritic and axonal arborization. Thus, we reared tadpoles in dark and light environments then used rhodamine dextran retrograde labeling to identify RGCs in the retina. When we compared RGC dendritic arbors from tadpoles reared in dark and light environments, we found no morphological differences, suggesting that physiological visual activity did not contribute to the morphological development of Xenopus RGC dendritic arbors.
Intrinsically photosensitive retinal ganglion cells
Gary E. Pickard,Patricia J. Sollars
Science China Life Sciences , 2010, DOI: 10.1007/s11427-010-0024-5
Abstract: A new mammalian photoreceptor was recently discovered to reside in the ganglion cell layer of the inner retina. These intrinsically photosensitive retinal ganglion cells (ipRGCs) express a photopigment, melanopsin that confers upon them the ability to respond to light in the absence of all rod and cone photoreceptor input. Although relatively few in number, ipRGCs extend their dendrites across large expanses of the retina making them ideally suited to function as irradiance detectors to assess changes in ambient light levels. Phototransduction in ipRGCs appears to be mediated by transient receptor potential channels more closely resembling the phototransduction cascade of invertebrate than vertebrate photoreceptors. ipRGCs convey irradiance information centrally via the optic nerve to influence several functions. ipRGCs are the primary retinal input to the hypothalamic suprachiasmatic nucleus (SCN), a circadian oscillator and biological clock, and this input entrains the SCN to the day/night cycle. ipRGCs contribute irradiance signals that regulate pupil size and they also provide signals that interface with the autonomic nervous system to regulate rhythmic gene activity in major organs of the body. ipRGCs also provide excitatory drive to dopaminergic amacrine cells in the retina, providing a novel basis for the restructuring of retinal circuits by light. Here we review the ground-breaking discoveries, current progress and directions for future investigation.
Remodeling and Tenacity of Inhibitory Synapses: Relationships with Network Activity and Neighboring Excitatory Synapses  [PDF]
Anna Rubinski?,Noam E. Ziv
PLOS Computational Biology , 2015, DOI: 10.1371/journal.pcbi.1004632
Abstract: Glutamatergic synapse size remodeling is governed not only by specific activity forms but also by apparently stochastic processes with well-defined statistics. These spontaneous remodeling processes can give rise to skewed and stable synaptic size distributions, underlie scaling of these distributions and drive changes in glutamatergic synapse size “configurations”. Where inhibitory synapses are concerned, however, little is known on spontaneous remodeling dynamics, their statistics, their activity dependence or their long-term consequences. Here we followed individual inhibitory synapses for days, and analyzed their size remodeling dynamics within the statistical framework previously developed for glutamatergic synapses. Similar to glutamatergic synapses, size distributions of inhibitory synapses were skewed and stable; at the same time, however, sizes of individual synapses changed considerably, leading to gradual changes in synaptic size configurations. The suppression of network activity only transiently affected spontaneous remodeling dynamics, did not affect synaptic size configuration change rates and was not followed by the scaling of inhibitory synapse size distributions. Comparisons with glutamatergic synapses within the same dendrites revealed a degree of coupling between nearby inhibitory and excitatory synapse remodeling, but also revealed that inhibitory synapse size configurations changed at considerably slower rates than those of their glutamatergic neighbors. These findings point to quantitative differences in spontaneous remodeling dynamics of inhibitory and excitatory synapses but also reveal deep qualitative similarities in the processes that control their sizes and govern their remodeling dynamics.
Fear Learning Increases the Number of Polyribosomes Associated with Excitatory and Inhibitory Synapses in the Barrel Cortex  [PDF]
Malgorzata Jasinska, Ewa Siucinska, Ewa Jasek, Jan A. Litwin, Elzbieta Pyza, Malgorzata Kossut
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0054301
Abstract: Associative fear learning, resulting from whisker stimulation paired with application of a mild electric shock to the tail in a classical conditioning paradigm, changes the motor behavior of mice and modifies the cortical functional representation of sensory receptors involved in the conditioning. It also induces the formation of new inhibitory synapses on double-synapse spines of the cognate barrel hollows. We studied density and distribution of polyribosomes, the putative structural markers of enhanced synaptic activation, following conditioning. By analyzing serial sections of the barrel cortex by electron microscopy and stereology, we found that the density of polyribosomes was significantly increased in dendrites of the barrel activated during conditioning. The results revealed fear learning-induced increase in the density of polyribosomes associated with both excitatory and inhibitory synapses located on dendritic spines (in both single- and double-synapse spines) and only with the inhibitory synapses located on dendritic shafts. This effect was accompanied by a significant increase in the postsynaptic density area of the excitatory synapses on single-synapse spines and of the inhibitory synapses on double-synapse spines containing polyribosomes. The present results show that associative fear learning not only induces inhibitory synaptogenesis, as demonstrated in the previous studies, but also stimulates local protein synthesis and produces modifications of the synapses that indicate their potentiation.
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