scholarly journals A retinal circuit generating a dynamic predictive code for orientated features

2018 ◽  
Author(s):  
Jamie Johnston ◽  
Sofie-Helene Seibel ◽  
Léa Simone Adele Darnet ◽  
Sabine Renninger ◽  
Michael Orger ◽  
...  

SummarySensory systems must reduce the transmission of redundant information to function efficiently. One strategy is to continuously adjust the sensitivity of neurons to suppress responses to common features of the input while enhancing responses to new ones. Here we image both the excitatory synaptic inputs and outputs of retinal ganglion cells to understand how such dynamic predictive coding is implemented in the analysis of spatial patterns. Synapses of bipolar cells become tuned to orientation through presynaptic inhibition generating lateral antagonism in the orientation domain. Individual ganglion cells receive excitatory synapses tuned to different orientations but feedforward inhibition generates a high-pass filter that only transmits the initial activation of these inputs, thereby removing redundancy. These results demonstrate how a dynamic predictive code can be implemented by circuit motifs common to many parts of the brain.

2018 ◽  
Author(s):  
Shai Sabbah ◽  
Carin Papendorp ◽  
Elizabeth Koplas ◽  
Marjo Beltoja ◽  
Cameron Etebari ◽  
...  

SummaryWe have explored the synaptic networks responsible for the unique capacity of intrinsically photosensitive retinal ganglion cells (ipRGCs) to encode overall light intensity. This luminance signal is crucial for circadian, pupillary and related reflexive responses light. By combined glutamate-sensor imaging and patch recording of postsynaptic RGCs, we show that the capacity for intensity-encoding is widespread among cone bipolar types, including OFF types.Nonetheless, the bipolar cells that drive ipRGCs appear to carry the strongest luminance signal. By serial electron microscopic reconstruction, we show that Type 6 ON cone bipolar cells are the dominant source of such input, with more modest input from Types 7, 8 and 9 and virtually none from Types 5i, 5o, 5t or rod bipolar cells. In conventional RGCs, the excitatory drive from bipolar cells is high-pass temporally filtered more than it is in ipRGCs. Amacrine-to-bipolar cell feedback seems to contribute surprisingly little to this filtering, implicating mostly postsynaptic mechanisms. Most ipRGCs sample from all bipolar terminals costratifying with their dendrites, but M1 cells avoid all OFF bipolar input and accept only ectopic ribbon synapses from ON cone bipolar axonal shafts. These are remarkable monad synapses, equipped with as many as a dozen ribbons and only one postsynaptic process.


2012 ◽  
Vol 29 (3) ◽  
pp. 157-168 ◽  
Author(s):  
CARLA J. ABBOTT ◽  
KUMIKO A. PERCIVAL ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT

AbstractRetinal ganglion cells receive excitatory synapses from bipolar cells and inhibitory synapses from amacrine cells. Previous studies in primate suggest that the strength of inhibitory amacrine input is greater to cells in peripheral retina than to foveal (central) cells. A comprehensive study of a large number of ganglion cells at different eccentricities, however, is still lacking. Here, we compared the amacrine and bipolar input to midget and parasol ganglion cells in central and peripheral retina of marmosets (Callithrix jacchus). Ganglion cells were labeled by retrograde filling from the lateral geniculate nucleus or by intracellular injection. Presumed amacrine input was identified with antibodies against gephyrin; presumed bipolar input was identified with antibodies against the GluR4 subunit of the AMPA receptor. In vertical sections, about 40% of gephyrin immunoreactive (IR) puncta were colocalized with GABAA receptor subunits, whereas immunoreactivity for gephyrin and GluR4 was found at distinct sets of puncta. The density of gephyrin IR puncta associated with ganglion cell dendrites was comparable for midget and parasol cells at all eccentricities studied (up to 2 mm or about 16 degrees of visual angle for midget cells and up to 10 mm or >80 degrees of visual angle for parasol cells). In central retina, the densities of gephyrin IR and GluR4 IR puncta associated with the dendrites of midget and parasol cells are comparable, but the average density of GluR4 IR puncta decreased slightly in peripheral parasol cells. These anatomical results indicate that the ratio of amacrine to bipolar input does not account for the distinct functional properties of parasol and midget cells or for functional differences between cells of the same type in central and peripheral retina.


2017 ◽  
Vol 89 (2) ◽  
pp. 84-103 ◽  
Author(s):  
Heidrun Kuhrt ◽  
Andreas Bringmann ◽  
Wolfgang Härtig ◽  
Gudrun Wibbelt ◽  
Leo Peichl ◽  
...  

Elephants are precocial mammals that are relatively mature as newborns and mobile shortly after birth. To determine whether the retina of newborn elephants is capable of supporting the mobility of elephant calves, we compared the retinal structures of 2 newborn elephants (1 African and 1 Asian) and 2 adult animals of both species by immunohistochemical and morphometric methods. For the first time, we present here a comprehensive qualitative and quantitative characterization of the cellular composition of the newborn and the adult retinas of 2 elephant species. We found that the retina of elephants is relatively mature at birth. All retinal layers were well discernible, and various retinal cell types were detected in the newborns, including Müller glial cells (expressing glutamine synthetase and cellular retinal binding protein; CRALBP), cone photoreceptors (expressing S-opsin or M/L-opsin), protein kinase Cα-expressing bipolar cells, tyrosine hydroxylase-, choline acetyltransferase (ChAT)-, calbindin-, and calretinin-expressing amacrine cells, and calbindin-expressing horizontal cells. The retina of newborn elephants contains discrete horizontal cells which coexpress ChAT, calbindin, and calretinin. While the overall structure of the retina is very similar between newborn and adult elephants, various parameters change after birth. The postnatal thickening of the retinal ganglion cell axons and the increase in ganglion cell soma size are explained by the increase in body size after birth, and the decreases in the densities of neuronal and glial cells are explained by the postnatal expansion of the retinal surface area. The expression of glutamine synthetase and CRALBP in the Müller cells of newborn elephants suggests that the cells are already capable of supporting the activities of photoreceptors and neurons. As a peculiarity, the elephant retina contains both normally located and displaced giant ganglion cells, with single cells reaching a diameter of more than 50 µm in adults and therefore being almost in the range of giant retinal ganglion cells found in aquatic mammals. Some of these ganglion cells are displaced into the inner nuclear layer, a unique feature of terrestrial mammals. For the first time, we describe here the occurrence of many bistratified rod bipolar cells in the elephant retina. These bistratified bipolar cells may improve nocturnal contrast perception in elephants given their arrhythmic lifestyle.


1998 ◽  
Vol 15 (1) ◽  
pp. 161-175 ◽  
Author(s):  
BARRY B. LEE ◽  
JAN KREMERS ◽  
TSAIYAO YEH

We have reinvestigated receptive-field structure of ganglion cells of the macaque parafovea using counterphase modulation of a bipartite field. Receptive fields were mapped with luminance, chromatic, and cone-isolating stimuli. Center sizes of middle (M) and long (L) wavelength cone opponent cells of the parvocellular (PC) pathway were consistent with previous estimates (Gaussian radii of 2–4 min of arc, corresponding to center diameters of 6–12 min of arc). We calculate that a large factor of the enlargement relative to cone radius could be blur due to the eye's natural optics. Maps were consistent with cone selectivity in surround mechanisms, which had radii of 5–8 min of arc. For magnocellular (MC) cells, center size estimates were also consistent with grating measurements from the literature (also Gaussian radii of 2–4 min of arc). The surround mechanism contributing the MC-cell frequency-doubled response to chromatic modulation appears to possess a subunit structure, and we speculate it derives from nonlinear summation of signals from M,L-cone opponent subunits, such as midget bipolar cells.


2012 ◽  
Vol 107 (7) ◽  
pp. 1795-1807 ◽  
Author(s):  
Ilya Buldyrev ◽  
Theresa Puthussery ◽  
W. Rowland Taylor

Different types of retinal ganglion cells represent distinct spatiotemporal filters that respond selectively to specific features in the visual input. Much about the circuitry and synaptic mechanisms that underlie such specificity remains to be determined. This study examines how N-methyl-d-aspartate (NMDA) receptor signaling combines with other excitatory and inhibitory mechanisms to shape the output of small-field OFF brisk-sustained ganglion cells (OFF-BSGCs) in the rabbit retina. We used voltage clamp to separately resolve NMDA, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), and inhibitory inputs elicited by stimulation of the receptive field center. Three converging circuits were identified. First is a direct glutamatergic input, arising from OFF cone bipolar cells (CBCs), which is mediated by synaptic NMDA and AMPA receptors. The NMDA input was saturated at 10% contrast, whereas the AMPA input increased monotonically up to 60% contrast. We propose that NMDA inputs selectively enhance sensitivity to low contrasts. The OFF bipolar cells, mediating this direct excitatory input, express dendritic kainate (KA) receptors, which are resistant to the nonselective AMPA/KA receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulfonamide disodium salt (NBQX), but are suppressed by a GluK1- and GluK3-selective antagonist, ( S)-1-(2-amino-2-carboxyethyl)-3-(2-carboxy-thiophene-3-yl-methyl)-5-methylpyrimidine-2,4-dione (UBP-310). The second circuit entails glycinergic crossover inhibition, arising from ON-CBCs and mediated by AII amacrine cells, which modulate glutamate release from the OFF-CBC terminals. The third circuit also comprises glycinergic crossover inhibition, which is driven by the ON pathway; however, this inhibition impinges directly on the OFF-BSGCs and is mediated by an unknown glycinergic amacrine cell that expresses AMPA but not KA receptors.


2010 ◽  
Vol 103 (6) ◽  
pp. 3184-3194 ◽  
Author(s):  
Sheila Nirenberg ◽  
Illya Bomash ◽  
Jonathan W. Pillow ◽  
Jonathan D. Victor

To make efficient use of their limited signaling capacity, sensory systems often use predictive coding. Predictive coding works by exploiting the statistical regularities of the environment—specifically, by filtering the sensory input to remove its predictable elements, thus enabling the neural signal to focus on what cannot be guessed. To do this, the neural filters must remove the environmental correlations. If predictive coding is to work well in multiple environments, sensory systems must adapt their filtering properties to fit each environment's statistics. Using the visual system as a model, we determine whether this happens. We compare retinal ganglion cell dynamics in two very different environments: white noise and natural. Because natural environments have more power than that of white noise at low temporal frequencies, predictive coding is expected to produce a suppression of low frequencies and an enhancement of high frequencies, compared with the behavior in a white-noise environment. We find that this holds, but only in part. First, predictive coding behavior is not uniform: most on cells manifest it, whereas off cells, on average, do not. Overlaid on this nonuniformity between cell classes is further nonuniformity within both cell classes. These findings indicate that functional considerations beyond predictive coding play an important role in shaping the dynamics of sensory adaptation. Moreover, the differences in behavior between on and off cell classes add to the growing evidence that these classes are not merely homogeneous mirror images of each other and suggest that their roles in visual processing are more complex than expected from the classic view.


2011 ◽  
Vol 6 (1) ◽  
pp. 31 ◽  
Author(s):  
Florentina Soto ◽  
Adam Bleckert ◽  
Renate Lewis ◽  
Yunhee Kang ◽  
Daniel Kerschensteiner ◽  
...  

2021 ◽  
Author(s):  
Mai Ahmed ◽  
Yutaka Kojima ◽  
Ichiro Masai

In the vertebrate retina, an interplay between retinal ganglion cells (RGCs), amacrine and bipolar cells establishes a synaptic layer called the inner plexiform layer (IPL). This circuit conveys signals from photoreceptors to visual centers in the brain. However, the molecular mechanisms involved in its development remain poorly understood. Striatin-interacting protein 1 (Strip1) is a core component of the STRIPAK complex, and it has shown emerging roles in embryonic morphogenesis. Here, we uncover the importance of Strip1 in inner retina development. Using zebrafish, we show that loss of Strip1 causes defects in IPL formation. In strip1 mutants, RGCs undergo dramatic cell death shortly after birth. Amacrine and bipolar cells subsequently invade the degenerating RGC layer, leading to a disorganized IPL. Thus, Strip1 promotes IPL formation through RGC maintenance. Mechanistically, zebrafish Strip1 interacts with its STRIPAK partner, Striatin3, to promote RGC survival by suppressing Jun-mediated apoptosis. In addition to its function in RGC maintenance, Strip1 is required for RGC dendritic patterning, which likely contributes to proper IPL formation. Taken together, we propose that a series of Strip1-mediated regulatory events coordinates inner retinal circuit formation by maintaining RGCs during development, which ensures proper positioning and neurite patterning of inner retinal neurons.


1998 ◽  
Vol 79 (4) ◽  
pp. 1869-1878 ◽  
Author(s):  
Daniel W. Crevier ◽  
Markus Meister

Crevier, Daniel W. and Markus Meister. Synchronous period-doubling in flicker vision of salamander and man. J. Neurophysiol. 79: 1869–1878, 1998. Periodic flashes of light have long served to probe the temporal properties of the visual system. Here we show that during rapid flicker of high contrast and intensity the eye reports to the brain only every other flash of light. In this regime, retinal ganglion cells of the salamander fire spikes on alternating flashes. Neurons across the entire retina are locked to the same flashes. The effect depends sharply on contrast and flash frequency. It results from a period-doubling bifurcation in retinal processing, and a simple model of nonlinear feedback reproduces the phenomenon. Pharmacological studies indicate that the critical feedback interactions require only cone photoreceptors and bipolar cells. Analogous period-doubling is observed in the human visual system. Under bright full-field flicker, the electroretinogram (ERG) shows a regime of period-doubling between 30 and 70 Hz. In visual evoked potentials from the occiput, the subharmonic component is even stronger. By analyzing the accompanying perceptual effects, we find that retinal period-doubling begins in the periphery of the visual field, and that it is the cause of a long mysterious illusory flicker pattern.


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