scholarly journals Energy saving in vision at the first synapse: The ON and OFF pathways measure temporal differences

2017 ◽  
Author(s):  
Bart M. ter Haar Romeny
Keyword(s):  
Visual System ◽  
Receptive Fields ◽  
Dendritic Tree ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Inner Plexiform Layer ◽  
Surveillance Camera ◽  
Starburst Amacrine Cells ◽  
Spatio Temporal ◽  
On And Off Pathways

AbstractThe inner plexiform layer (IPL) of mammalian retina has a precise bisublaminar organization in an inner on- and an outer off-layer, innervated by spatially segregated on- and off-cone bipolar cell inputs. Also, the processes of starburst amacrine cells are segregated into on and off sublaminae of the IPL. Distances between overlapping on-off pair retinal ganglion cell dendritic tree centers are markedly smaller than between on-on or off-off centers, indicating simultaneously sampling the same space. Despite dekades of research, no good model exists for the role of the on- and off pathways. Here I propose that the on- and off pairs are temporally subtracted, with one channel delayed in time, likely in a higher cortical center. The on- and off receptive fields give at every retinal location an I+ and I-signal, where I is intensity, velocity, color. Subsequent frame subtraction is a basis function of every surveillance camera for vision, and in MPEG video/sound compression. The model explains the many phenomena observed when the retinal image is stabilized. The separation of layers in the LGN fits with the notion of a time delay at higher cortical level. The directionalty observed in micro-saccades is typically perpendicular to the main edges in the scene. Precise measurement of spatio-temporal receptive field kernels shows that time is processed in the visual system as a real-time process, i.e. with a logarithmic time axis. As only contours and textures are transmitted, it is a very effective design strategy of the visual system to conserve energy, in a brain that typically uses 25 Watt and very low neuron firing frequencies. The higher visual centers perform the fill-in (inpainting) with such efficiency, that the subtraction always goes unnoticed.

scholarly journals Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Thomas A Ray ◽  
Suva Roy ◽  
Christopher Kozlowski ◽  
Jingjing Wang ◽  
Jon Cafaro ◽  
...  
Keyword(s):  
Synapse Formation ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Surface Protein ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Mouse Retina ◽  
Inner Plexiform Layer ◽  
Starburst Amacrine Cells ◽  
Developing Neurons

A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.

The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

1996 ◽  
Vol 13 (6) ◽  
pp. 1099-1107 ◽  
Author(s):  
Péter Buzás ◽  
Sára Jeges ◽  
Robert Gábriel
Keyword(s):  
Ganglion Cell ◽  
Cross Sections ◽  
Information Transfer ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Flow Through

AbstractThe main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.

Dendritic morphology and tracer-coupling pattern of physiologically identified transient uniformity detector ganglion cells in rabbit retina

2010 ◽  
Vol 27 (5-6) ◽  
pp. 159-170 ◽  
Author(s):  
BENJAMIN SIVYER ◽  
DAVID I. VANEY
Keyword(s):  
Dendritic Tree ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Dendritic Morphology ◽  
Dendritic Arbor ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Functional Identification ◽  
Unique Type ◽  
Coupling Pattern

AbstractTransient uniformity detectors (UDs) are a unique type of retinal ganglion cell (RGC) whose maintained firing is transiently suppressed by all types of visual stimuli. In this study, we have characterized the dendritic morphology and tracer-coupling pattern of UDs that were labeled by loose-seal electroporation of Neurobiotin following functional identification in the isolated rabbit retina. The UDs have a bistratified dendritic tree, branching near the margins of the inner plexiform layer in stratum 1 (part of the OFF sublamina) and stratum 4/5 (part of the ON sublamina). Characteristically, many of the distal dendrites in the OFF arbor do not terminate there but dive recurrently back to the ON arbor. As a consequence, the ON dendritic arbor is usually twice as large as the OFF dendritic arbor in area. The UDs sometimes show homologous tracer coupling to neighboring RGCs with the same morphology, and from this material, we estimate that the UDs have a threefold dendritic field overlap and a maximum density of ~100 cells/mm2 on the peak visual streak, accounting for ~2% of RGCs in rabbit retina. The UDs also show strong heterologous tracer coupling to a novel type of amacrine cell that costratifies with the ON arbor of the UD. Consistent with their unistratified medium-field morphology, these St4/5 amacrine cells appear to be GABAergic: their somata are immunopositive for GABA but immunonegative for glycine and glycine transporter 1. We compare the dendritic morphology of the UDs to that of other types of bistratified RGCs described in rabbit retina and note that the stratification levels and distinctive recurrent dendrites closely resemble those of the “ON bistratified diving” RGCs. This raises the possibility that there are two types of RGCs with distinctive physiological properties that have almost identical bistratified dendritic morphologies.

The type 1 polyaxonal amacrine cells of the rabbit retina: A tracer-coupling study

2004 ◽  
Vol 21 (2) ◽  
pp. 145-155 ◽  
Author(s):  
LAYNE L. WRIGHT ◽  
DAVID I. VANEY
Keyword(s):  
Dendritic Tree ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Field Size ◽  
Equivalent Diameter ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Visual Streak ◽  
Field Area

The type 1 polyaxonal (PA1) cell is a distinct type of axon-bearing amacrine cell whose soma commonly occupies an interstitial position in the inner plexiform layer; the proximal branches of the sparse dendritic tree produce 1–4 axon-like processes, which form an extensive axonal arbor that is concentric with the smaller dendritic tree (Dacey, 1989; Famiglietti, 1992a,b). In this study, intracellular injections of Neurobiotin have revealed the complete dendritic and axonal morphology of the PA1 cells in the rabbit retina, as well as labeling the local array of PA1 cells through homologous tracer coupling. The dendritic-field area of the PA1 cells increased from a minimum of 0.15 mm2 (0.44-mm equivalent diameter) on the visual streak to a maximum of 0.67 mm2 (0.92-mm diameter) in the far periphery; the axonal-field area also showed a 3-fold variation across the retina, ranging from 3.1 mm2 (2.0-mm diameter) to 10.2 mm2 (3.6-mm diameter). The increase in dendritic- and axonal-field size was accompanied by a reduction in cell density, from 60 cells/mm2 in the visual streak to 20 cells/mm2 in the far periphery, so that the PA1 cells showed a 12 times overlap of their dendritic fields across the retina and a 200–300 times overlap of their axonal fields. Consequently, the axonal plexus was much denser than the dendritic plexus, with each square millimeter of retina containing ∼100 mm of dendrites and ∼1000 mm of axonal processes. The strong homologous tracer coupling revealed that ∼45% of the PA1 somata were located in the inner nuclear layer, ∼50% in the inner plexiform layer, and ∼5% in the ganglion cell layer. In addition, the Neurobiotin-injected PA1 cells sometimes showed clear heterologous tracer coupling to a regular array of small ganglion cells, which were present at half the density of the PA1 cells. The PA1 cells were also shown to contain elevated levels of γ-aminobutyric acid (GABA), like other axon-bearing amacrine cells.

scholarly journals In vivo Morphometry of Inner Plexiform Layer (IPL) Stratification in the Human Retina With Visible Light Optical Coherence Tomography

2021 ◽  
Vol 15 ◽  
Author(s):  
Tingwei Zhang ◽  
Aaron M. Kho ◽  
Vivek J. Srinivasan
Keyword(s):  
Optical Coherence Tomography ◽  
Visual System ◽  
Visible Light ◽  
Human Subjects ◽  
Plexiform Layer ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Optical Coherence ◽  
On And Off Pathways

From the bipolar cells to higher brain visual centers, signals in the vertebrate visual system are transmitted along parallel on and off pathways. These two pathways are spatially segregated along the depth axis of the retina. Yet, to our knowledge, there is no way to directly assess this anatomical stratification in vivo. Here, employing ultrahigh resolution visible light Optical Coherence Tomography (OCT) imaging in humans, we report a stereotyped reflectivity pattern of the inner plexiform layer (IPL) that parallels IPL stratification. We characterize the topography of this reflectivity pattern non-invasively in a cohort of normal, young adult human subjects. This proposed correlate of IPL stratification is accessible through non-invasive ocular imaging in living humans. Topographic variations should be carefully considered when designing studies in development or diseases of the visual system.

Light responses from one type of ON-OFF amacrine cells in the rabbit retina

1995 ◽  
Vol 74 (6) ◽  
pp. 2460-2468 ◽  
Author(s):  
R. F. Dacheux ◽  
E. Raviola
Keyword(s):  
Light Adaptation ◽  
Receptive Fields ◽  
Central Area ◽  
Plexiform Layer ◽  
Light Response ◽  
Amacrine Cells ◽  
Wide Field ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Light Responses

1. The light responses from one type of ON-OFF amacrine cell were recorded intracellularly in the superfused rabbit retina under various conditions of light adaptation. These recordings were obtained from cells located in a central area. 5-7 mm inferior and directly below the optic nerve head. 2. ON-OFF amacrine cells responded to the initiation and termination of light stimuli with transient depolarizations. Their receptive fields were approximately 0.8-1 mm diam and did not exhibit antagonistic center-and-surround organization. 3. The cells received rod input because they responded to very dim scotopic stimuli. With prolonged dark adaptation, the cells became more sensitive to the initiation than termination of the stimulus, because the ON component of the light response had a lower threshold than the OFF component. 4. The cells continued to respond to test flashes when the retina was adapted to a background illumination of rod-saturating intensity. Thus ON-OFF amacrine cells also receive cone input. Under these photopic conditions, a secondary afterpotential was observed following the OFF component. Its characteristics were different from those of the rod aftereffect reported in other retinal cells of the rabbit because its latency and amplitude changed with increasing stimulus intensity. 5. Intracellular injections of horseradish peroxidase showed that the recordings were obtained from a class of ON-OFF amacrine cells whose wide-field, unistratified dendrites were rigorously confined to the middle of the inner plexiform layer or stratum 3. 6. The conspicuous rod and cone inputs into a class of amacrine cells that are connected neither to rod bipolars nor to All amacrine cells strongly support the idea that in the rabbit the rod pathway uses cone bipolars as interneurons to distribute scotopic signals to ganglion and cone-driven amacrine cells.

Displaced starburst amacrine cells of the rabbit retina contain the 67-kDa isoform, but not the 65-kDa isoform, of glutamate decarboxylase

1995 ◽  
Vol 12 (6) ◽  
pp. 1053-1061 ◽  
Author(s):  
Christopher Brandon ◽  
Mark H. Criswell
Keyword(s):  
Choline Acetyltransferase ◽  
Glutamate Decarboxylase ◽  
Lucifer Yellow ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Biosynthetic Enzyme ◽  
Starburst Amacrine Cells

AbstractThe cholinergic identity of retinal starburst amacrine neurons is well established, but recent evidence suggests that these cells are GABAergic as well. Confirmation of this dual transmitter function requires the demonstration of glutamate decarboxylase (GAD), the biosynthetic enzyme for GABA, within starburst cells. The current work was undertaken to determine whether rabbit retinal starburst amacrine neurons contain either of the two known isoforms of GAD. To do this, we have examined the localization of the following: (1) the 65-kDa isoform of GAD; (2) the 67-kDa isoform of GAD; (3) choline acetyltransferase; and (4) the fluorescent dye DAPI, a marker for cholinergic amacrine cells. In addition, we labeled displaced starburst neurons directly, by injecting them with Lucifer Yellow in vitro. Four strata within the inner plexiform layer contained immunoreactive GAD65. A non-GAD65-immunoreactive zone separated the two innermost strata (G3 and G4); this zone contained (1) the dendrites of individual Lucifer Yellow-injected, displaced starburst amacrine cells; (2) dendrites immunoreactive for choline acetyltransferase; and (3) processes of DAPI-labeled amacrine cells. Immunoreactive GAD67 appeared in the same strata that contained GAD65, and in at least two additional strata, one of which lay at precisely the same depth as the proximal cholinergic stratum. In addition, the somas of displaced starburst cells were strongly immunoreactive for GAD67, but not for GAD65. These results demonstrate (1) that displaced starburst amacrine cells contain the 67-kDa isoform of GAD, but not the 65-kDa isoform; and (2) that the dendrites of starburst (67-kDa GAD) amacrines, and the dendrites of 65-kDa-GAD-containing amacrines, occupy different strata within the inner plexiform layer. Thus, displaced starburst cells do contain GAD, and can, presumably, manufacture GABA. The reasons for their preferential use of the 67-kDa GAD isoform remain to be elucidated.

scholarly journals Bistratified starburst amacrine cells in Sox2 conditional knockout mouse retina display ON and OFF responses

2018 ◽  
Vol 120 (4) ◽  
pp. 2121-2129 ◽  
Author(s):  
Todd L. Stincic ◽  
Patrick W. Keeley ◽  
Benjamin E. Reese ◽  
W. Rowland Taylor
Keyword(s):  
Transcription Factor ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Conditional Knockout ◽  
Physiological Data ◽  
Mouse Retina ◽  
Inner Plexiform Layer ◽  
Environmental Signals ◽  
Starburst Amacrine Cells

Cell-intrinsic factors, in conjunction with environmental signals, guide migration, differentiation, and connectivity during early development of neuronal circuits. Within the retina, inhibitory starburst amacrine cells (SBACs) comprise ON types with somas in the ganglion cell layer (GCL) and dendrites stratifying narrowly in the inner half of the inner plexiform layer (IPL) and OFF types with somas in the inner nuclear layer (INL) and dendrites stratifying narrowly in the outer half of the IPL. The transcription factor Sox2 is crucial to this subtype specification. Without Sox2, many ON-type SBACs destined for the GCL settle in the INL while many that reach the GCL develop bistratified dendritic arbors. This study asked whether ON-type SBACs in Sox2-conditional knockout retinas exhibit selective connectivity only with ON-type bipolar cells or their bistratified morphology allows them to connect to both ON and OFF bipolar cells. Physiological data demonstrate that these cells receive ON and OFF excitatory inputs, indicating that the ectopically stratified dendrites make functional synapses with bipolar cells. The excitatory inputs were smaller and more transient in Sox2-conditional knockout compared with wild type; however, inhibitory inputs appeared largely unchanged. Thus dendritic stratification, rather than cellular identification, may be the major factor that determines ON vs. OFF connectivity. NEW & NOTEWORTHY Conditional knockout of the transcription factor Sox2 during early embryogenesis converts a monostratifying starburst amacrine cell into a bistratifying starburst cell. Here we show that these bistratifying starburst amacrine cells form functional synaptic connections with both ON and OFF bipolar cells. This suggests that normal ON vs. OFF starburst connectivity may not require distinct molecular specification. Proximity alone may be sufficient to allow formation of functional synapses.

scholarly journals Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact

2017 ◽  
Author(s):  
Thomas A. Ray ◽  
Suva Roy ◽  
Christopher Kozlowski ◽  
Jingjing Wang ◽  
Jon Cafaro ◽  
...  
Keyword(s):  
Synapse Formation ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Surface Protein ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Mouse Retina ◽  
Inner Plexiform Layer ◽  
Starburst Amacrine Cells ◽  
Developing Neurons

Impact statementSelective synapse formation in a retinal motion-sensitive circuit is orchestrated by starburst amacrine cells, which use homotypic interactions to initiate formation of a dendritic scaffold that recruits projections from circuit partners.SUMMARYA common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially-migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.

Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors

2000 ◽  
Vol 17 (5) ◽  
pp. 743-752 ◽  
Author(s):  
KENT T. KEYSER ◽  
MARGARET A. MACNEIL ◽  
NINA DMITRIEVA ◽  
FAN WANG ◽  
RICHARD H. MASLAND ◽  
...  
Keyword(s):  
Nicotinic Acetylcholine Receptors ◽  
Acetylcholine Receptors ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Receptor Expression ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Nicotinic Acetylcholine ◽  
Starburst Amacrine Cells

Acetylcholine (ACh) in the vertebrate retina affects the response properties of many ganglion cells, including those that display directional selectivity. Three β and eight α subunits of neuronal nicotinic acetylcholine receptors (nAChRs) have been purified and antibodies have been raised against many of them. Here we describe biochemical and immunocytochemical studies of nAChRs in the rabbit retina. Radioimmunoassay and Western blot analysis demonstrated that many of the nAChRs recognized by a monoclonal antibody (mAb210) contain β2 subunits, some of which are in combination with α3 and possibly other subunits. MAb210-immunoreactive cells in the inner nuclear layer (INL) were 7–14 μm in diameter and were restricted to the innermost one or two tiers of cells, although occasional cells were found in the middle of the INL. At least 60% of the cells in the ganglion cell layer (GCL) in the visual streak displayed mAb210 immunoreactivity; these neurons ranged from 7–18 μm in diameter. The dendrites of cells in both the INL and GCL could sometimes be followed until they entered one of two dense, poorly defined, bands of processes in the inner plexiform layer (IPL) that overlap the arbors of the cholinergic starburst cells. Parvalbumin and serotonin-positive neurons did not exhibit nAChR immunoreactivity. Although the level of receptor expression appeared to be low, mAb210 immunoreactivity was observed in some of the ChAT-positive (starburst) amacrine cells.

Sign in / Sign up

Export Citation Format

Share Document