Synaptic inputs to broad thorny ganglion cells in macaque retina.
12 Apr 2021-The Journal of Comparative Neurology (John Wiley & Sons, Ltd)-Vol. 529, Iss: 11, pp 3098-3111
TL;DR: A connectome from the central macaque retina was generated by serial block-face scanning electron microscopy, and a broad thorny cell was reconstructed, and its synaptic inputs were analyzed as mentioned in this paper.
Abstract: In primates, broad thorny retinal ganglion cells are highly sensitive to small, moving stimuli. They have tortuous, fine dendrites with many short, spine-like branches that occupy three contiguous strata in the middle of the inner plexiform layer. The neural circuits that generate their responses to moving stimuli are not well-understood, and that was the goal of this study. A connectome from central macaque retina was generated by serial block-face scanning electron microscopy, a broad thorny cell was reconstructed, and its synaptic inputs were analyzed. It received fewer than 2% of its inputs from both ON and OFF types of bipolar cells; the vast majority of its inputs were from amacrine cells. The presynaptic amacrine cells were reconstructed, and seven types were identified based on their characteristic morphology. Two types of narrow-field cells, knotty bistratified type 1 and wavy multistratified type 2, were identified. Two types of medium-field amacrine cells, ON starburst and spiny, were also presynaptic to the broad thorny cell. Three types of wide-field amacrine cells, wiry type 2, stellate wavy and semilunar type 2, also made synapses onto the broad thorny cell. Physiological experiments using a macaque retinal preparation in vitro confirmed that broad thorny cells received robust excitatory input from both the ON and the OFF pathways. Given the paucity of bipolar cell inputs, it is likely that amacrine cells provided much of the excitatory input, in addition to inhibitory input. This article is protected by copyright. All rights reserved.
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TL;DR: In this paper, the authors used antibodies against the AT-rich binding protein 1 (Satb1, a protein which is expressed by on-off direction-selective ganglion cells in mouse retina) to study Satb1 expression in the retina of marmosets, macaques, and humans.
Abstract: Recent advances in single-cell RNA sequencing have enabled the molecular distinction of ganglion cell populations in mammalian retinas. Here we used antibodies against the transcription factor special AT-rich binding protein 1 (Satb1, a protein which is expressed by on-off direction-selective ganglion cells in mouse retina) to study Satb1 expression in the retina of marmosets (Callithrix jacchus), macaques (Macaca fascicularis), and humans. In all species, Satb1 was exclusively expressed in retinal ganglion cells. The Satb1 cells made up ∼2% of the ganglion cell population in the central retina of all species, rising to a maximum ∼7% in peripheral marmoset retina. Intracellular injections in marmoset and macaque retinas revealed that most Satb1 expressing ganglion cells are widefield ganglion cells. In marmoset, Satb1 cells have a densely branching dendritic tree and include broad and narrow thorny, recursive bistratified, and parasol cells, all of which show some costratification with the outer or inner cholinergic amacrine cells. The recursive bistratified cells showed the strongest costratification but did not show extensive cofasciculation as reported for on-off direction-selective ganglion cells in rabbit and rodent retinas. In macaque, Satb1 was not expressed in recursive bistratified cells, but in large sparsely branching cells. Our findings further support the idea that the expression of transcription factors in retinal ganglion cells is not conserved across Old World (human and macaque) and New World (marmoset) primates and provides a further step to link a molecular marker with specific cell types.
6 citations
TL;DR: In this paper , a connectomic reconstruction of the primate ON SAC circuit from a serial electron microscopy volume of the macaque central retina is presented, showing that the structural basis for the SACs' ability to confer directional selectivity on postsynaptic neurons is conserved.
6 citations
TL;DR: In this paper , three sets of horizontal, ultrathin sections through central macaque retina were collected using serial block-face scanning electron microscopy to investigate their synaptic inputs, and they were identified as the displaced M1 type of ipRGCs based on this morphology and on the high density of granules in their somas.
Abstract: Ganglion cells are the projection neurons of the retina. Intrinsically photosensitive retinal ganglion cells (ipRGCs) express the photopigment melanopsin and also receive input from rods and cones via bipolar cells and amacrine cells. In primates, multiple types of ipRGCs have been identified. The ipRGCs with somas in the ganglion cell layer have been studied extensively, but less is known about those with somas in the inner nuclear layer, the "displaced" cells. To investigate their synaptic inputs, three sets of horizontal, ultrathin sections through central macaque retina were collected using serial block-face scanning electron microscopy. One displaced ipRGC received nearly all of its excitatory inputs from ON bipolar cells and would therefore be expected to have ON responses to light. In each of the three volumes, there was also at least one cell that had a large soma in the inner nuclear layer, varicose axons and dendrites with a large diameter that formed large, extremely sparse arbor in the outermost stratum of the inner plexiform layer. They were identified as the displaced M1 type of ipRGCs based on this morphology and on the high density of granules in their somas. They received extensive input from amacrine cells, including the dopaminergic type. The vast majority of their excitatory inputs were from OFF bipolar cells, including two subtypes with extensive input from the primary rod pathway. They would be expected to have OFF responses to light stimuli below the threshold for melanopsin or soon after the offset of a light stimulus.
1 citations
TL;DR: In this article , the authors used antibodies against carbonic anhydrase 8 (CA8) and intracellular injections of the liphilic dye DiI to show that CA8 selectively labels OFF parasol cells in macaque retina.
1 citations
TL;DR: In this paper , a volume of serial, ultrathin sections of central macaque retina in which many neurons that ramify in the inner plexiform layer (IPL) had been reconstructed previously was analyzed.
Abstract: Microglial cells are the primary resident immune cells in the retina. In healthy adults, they are ramified; that is, they have extensive processes that move continually. In adult retinas, microglia maintain the normal structure and function of neurons and other glial cells, but the mechanism underlying this process is not well-understood. In the mouse hippocampus, microglia engulf small pieces of axons and presynaptic terminals via a process called trogocytosis. Here we report that microglia in the adult macaque retina also engulf pieces of neurons and glial cells, but not at sites of synapses. We analyzed microglia in a volume of serial, ultrathin sections of central macaque retina in which many neurons that ramify in the inner plexiform layer (IPL) had been reconstructed previously. We surveyed the IPL and identified the somas of microglia by their small size and scant cytoplasm. We then reconstructed the microglia and studied their interactions with other cells. We found that ramified microglia frequently ingested small pieces of each major type of inner retinal neuron and Müller glial cells via trogocytosis. There were a few instances where the interactions took place near synapses, but the synapses, themselves, were never engulfed. If trogocytosis by retinal microglia plays a role in synaptic remodeling, it was not apparent from the ultrastructure. Instead, we propose that trogocytosis enables these microglia to present antigens derived from normal inner retinal cells and, when activated, they would promote antigen-specific tolerance.
References
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TL;DR: The retinae of monkey and man have been studied by electron microscopy to identify cell types, their processes and synaptic contacts, and a model of the retina, based on the described anatomy, is presented and correlated with ganglion cell physiology.
Abstract: 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.
963 citations
TL;DR: The structure of the human, but mainly of the rhesus monkey, retina as examined by Golgi-staining techniques is described and interpreted on evidence from both light and electron microscopy.
Abstract: The structure of the human, but mainly of the rhesus monkey, retina as examined by Golgi-staining techniques is described and interpreted on evidence from both light and electron microscopy. One type of rod bipolar cell and two types of cone bipolar cell are recognized. The rod bipolar is exclusively connected to rods. The midget bipolar is postsynaptic to only one cone but each cone is also presynaptic to a diffuse cone (flat) bipolar. Such flat bipolar cells are in synaptic relationship with about seven cones. No other bipolar cell types have been found. The brush bipolar of Polyak is interpreted as probably a distorted rod bipolar, while Polyak's centrifugal bipolar is a misinterpretation of the morphology of diffuse amacrine cells. When presumptive centrifugal bipolars were observed they appeared to be a developmental stage of amacrine cells. In the outer plexiform layer two types of horizontal cell have been defined. Each type of horizontal cell has a single axon and two kinds of horizontal cell axon terminals are recognized. In the inner plexiform layer there are two main classes of amacrine cells: the stratified amacrines and the diffuse amacrines. Each class of amacrine has a wide variety of shapes. Polyak's midget ganglion cell is confirmed and his five other kinds of ganglion cell are classified into diffuse and stratified ganglion cells according to the level at which their dendrites branch within the inner plexiform layer. A fuller summary is given by the diagram and in the legend of figure 98, p. 174. A new type of midget bipolar is described in the Appendix (p. 177).
552 citations
TL;DR: Quantitative assessment of response transiency shows that this measure reliably differentiates these two classes of retinal ganglion cells, and indicates that color-opponent and broad-band cells respond in a sustained fashion and in a transient fashion to visual stimuli.
Abstract: 1. Extracellular single-unit recordings were undertaken in the retina of the rhesus monkey in order to assess the receptive-field properties of those ganglion cells which project to the superior co...
351 citations
TL;DR: Camera lucida drawings and photography were used to classify the impregnated neurons into 3 types of horizontal cell, 9 types of bipolar cell, 24 basic types of amacrine cell, a single type of interplexiform cell, and 18 types of ganglion cell.
Abstract: Golgi techniques have been applied to post mortem specimens of human retina. Analysis was possible on 150 human retinas processed and viewed by light microscopy as wholemounts. Camera lucida drawings and photography were used to classify the impregnated neurons into 3 types of horizontal cell, 9 types of bipolar cell, 24 basic types of amacrine cell, a single type of interplexiform cell, and 18 types of ganglion cell. We have distinguished two types of midget bipolar cell: fmB (flat) and imB (invaginating). In central retina, both types are typically single-headed, each clearly contacting a single cone. Peripherally, they may be two- or even three-headed, obviously contacting more than one cone. Two types of small-field diffuse cone bipolars occurring as flat and invaginating varieties are found across the entire retina from fovea to far periphery. The single rod bipolar type appears about 1 mm from the fovea and increases in dendritic tree diameter from there into the far periphery. The putative "ON-center" blue cone bipolar and the giant bistratified bipolar first described by Mariani are also present in human retina and we add two previously undescribed bipolar cell types: a putative giant diffuse invaginating and a candidate "OFF-center" blue cone bipolar. Taking into account the variation of cell size with eccentricity at all points on the retina, we observed three distinct varieties of horizontal cell. The HI is the well known, long-axon-bearing cell of Polyak. HII is the more recently described multibranched, wavy-axoned horizontal cell. The third variety, HIII, introduced here, has been separated from the HI type on morphological criteria of having a larger, more asymmetrical dendritic field and in contacting 30% more cones than the HI at any point on the retina. Amacrine cells proved to be most diverse in morphology. Many of the amacrine cell types that have been described in cat retina (Kolb et al., '81: Vision Res. 21; 1081-1114) were seen in this study. Where there are no equivalent cells in cat, we have adopted the descriptive terminology used by Mariani in monkey retina. Thus eight varieties of small-field amacrines (under 100 microns dendritic trees), eight varieties of medium-field cells (100-500 microns dendritic span), and eight large-field varieties (over 500 microns dendritic trees) have been classified. Often a broadly described variety of amacrine cell can be subdivided into as many as three subtypes dependent on stratification levels of their dendrites in the inner plexiform layer.(ABSTRACT TRUNCATED AT 400 WORDS)
346 citations
TL;DR: A process termed retrograde photodynamics was described that allowed us to rapidly make the link between morphology, physiology, and connectivity for ganglion cells in the macaque retina that project to the lateral geniculate nucleus (LGN).
281 citations