scholarly journals Conserved Circuits for Direction Selectivity in the Primate Retina

2021 ◽  
Author(s):  
Sara S Patterson ◽  
Briyana N Bembry ◽  
Marcus A Mazzaferri ◽  
Maureen Neitz ◽  
Fred Rieke ◽  
...  
Keyword(s):  
Ganglion Cells ◽  
Selective Inhibition ◽  
Direction Selectivity ◽  
Structural Basis ◽  
Motion Processing ◽  
Retinal Ganglion ◽  
Accessory Optic System ◽  
Motion Direction ◽  
Open Question ◽  
Starburst Amacrine Cell

The detection of motion direction is a fundamental visual function and a classic model for neural computation. In the non-primate mammalian retina, direction selectivity arises in starburst amacrine cell (SAC) dendrites, which provide selective inhibition to ON and ON-OFF direction selective retinal ganglion cells (dsRGCs). While SACs are present in primates, their connectivity is unknown and the existence of primate dsRGCs remains an open question. Here we present a connectomic reconstruction of the primate ON SAC circuit from a serial electron microscopy volume of macaque central retina. We show that the structural basis for the SAC's ability to compute and confer directional selectivity on post-synaptic RGCs is conserved in primates and that SACs selectively target a single ganglion cell type, a candidate homolog to the mammalian ON-sustained dsRGCs that project to the accessory optic system and contribute to gaze-stabilizing reflexes. These results indicate that the capacity to compute motion direction is present in the retina, far earlier in the primate visual system than classically thought, and they shed light on the distinguishing features of primate motion processing by revealing the extent to which ancestral motion circuits are conserved.

scholarly journals Origins of direction selectivity in the primate retina

2021 ◽  
Author(s):  
Yeon Jin Kim ◽  
Beth Peterson ◽  
Joanna Crook ◽  
Hannah Joo ◽  
Jiajia Wu ◽  
...  
Keyword(s):  
Neural Coding ◽  
Amacrine Cell ◽  
Cell Types ◽  
Macaque Monkey ◽  
Direction Selectivity ◽  
Bipolar Cells ◽  
Motion Processing ◽  
Motion Direction ◽  
Motion Sensitivity ◽  
Starburst Amacrine Cell

Abstract From mouse to primate, there is a striking discontinuity in our current understanding of the neural coding of motion direction. In non-primate mammals, directionally selective cell types and circuits are a signature feature of the retina, situated at the earliest stage of the visual process1,2. In primates, by contrast, direction selectivity is a hallmark of motion processing areas in visual cortex3,4, but has not been found in the retina, despite significant effort5,6. Here we combined functional recordings of light-evoked responses and connectomic reconstruction to identify diverse direction-selective cell types in the macaque monkey retina with distinctive physiological properties and synaptic motifs. This circuitry includes an ON-OFF ganglion cell type, a spiking, ON-OFF poly-axonal amacrine cell and the starburst amacrine cell, all of which show direction selectivity. Moreover, we found unexpectedly that macaque starburst cells possess a strong, non-GABAergic, antagonistic surround mediated by input from excitatory bipolar cells that is critical for the generation of radial motion sensitivity in these cells. Our findings open a new door to investigation of a novel circuitry that computes motion direction in the primate visual system.

Neural Mechanisms of Motion Processing in the Mammalian Retina

2018 ◽  
Vol 4 (1) ◽  
pp. 165-192 ◽  
Author(s):  
Wei Wei
Keyword(s):  
Visual Motion ◽  
Ganglion Cells ◽  
Direction Selectivity ◽  
Neural Mechanisms ◽  
Motion Processing ◽  
Retinal Ganglion ◽  
Multiple Streams ◽  
Neural Basis ◽  
Population Activity ◽  
Motion Features

Visual motion on the retina activates a cohort of retinal ganglion cells (RGCs). This population activity encodes multiple streams of information extracted by parallel retinal circuits. Motion processing in the retina is best studied in the direction-selective circuit. The main focus of this review is the neural basis of direction selectivity, which has been investigated in unprecedented detail using state-of-the-art functional, connectomic, and modeling methods. Mechanisms underlying the encoding of other motion features by broader RGC populations are also discussed. Recent discoveries at both single-cell and population levels highlight the dynamic and stimulus-dependent engagement of multiple mechanisms that collectively implement robust motion detection under diverse visual conditions.

scholarly journals Global motion processing by populations of direction-selective retinal ganglion cells

2019 ◽  
Author(s):  
Jon Cafaro ◽  
Joel Zylberberg ◽  
Greg Field
Keyword(s):  
Ganglion Cells ◽  
Neural Population ◽  
Mouse Retina ◽  
Motion Processing ◽  
High Temporal Resolution ◽  
Retinal Ganglion ◽  
Global Motion ◽  
Local Motion ◽  
Motion Direction ◽  
Temporal Precision

AbstractSimple stimuli have been critical to understanding neural population codes in sensory systems. Yet it remains necessary to determine the extent to which this understanding generalizes to more complex conditions. To explore this problem, we measured how populations of direction-selective ganglion cells (DSGCs) from mouse retina respond to a global motion stimulus with its direction and speed changing dynamically. We then examined the encoding and decoding of motion direction in both individual and populations of DSGCs. Individual cells integrated global motion over ~200 ms, and responses were tuned to direction. However, responses were sparse and broadly tuned, which severely limited decoding performance from small DSGC populations. In contrast, larger populations compensated for response sparsity, enabling decoding with high temporal precision (<100 ms). At these timescales, correlated spiking was minimal and had little impact on decoding performance, unlike results obtained using simpler local motion stimuli decoded over longer timescales. We use these data to define different DSGC population decoding regimes that utilize or mitigate correlated spiking to achieve high spatial versus high temporal resolution.

scholarly journals GABA release selectively regulates synapse development at distinct inputs on direction-selective retinal ganglion cells

2018 ◽  
Vol 115 (51) ◽  
pp. E12083-E12090 ◽  
Author(s):  
Adam Bleckert ◽  
Chi Zhang ◽  
Maxwell H. Turner ◽  
David Koren ◽  
David M. Berson ◽  
...  
Keyword(s):  
Ganglion Cells ◽  
Selective Reduction ◽  
Amacrine Cells ◽  
Gaba Release ◽  
Direction Selectivity ◽  
Inhibitory Synapses ◽  
Retinal Ganglion ◽  
Gabaergic Transmission ◽  
Starburst Amacrine Cells ◽  
Receptor Clusters

Synaptic inhibition controls a neuron’s output via functionally distinct inputs at two subcellular compartments, the cell body and the dendrites. It is unclear whether the assembly of these distinct inhibitory inputs can be regulated independently by neurotransmission. In the mammalian retina, γ-aminobutyric acid (GABA) release from starburst amacrine cells (SACs) onto the dendrites of on–off direction-selective ganglion cells (ooDSGCs) is essential for directionally selective responses. We found that ooDSGCs also receive GABAergic input on their somata from other amacrine cells (ACs), including ACs containing the vasoactive intestinal peptide (VIP). When net GABAergic transmission is reduced, somatic, but not dendritic, GABAA receptor clusters on the ooDSGC increased in number and size. Correlative fluorescence imaging and serial electron microscopy revealed that these enlarged somatic receptor clusters are localized to synapses. By contrast, selectively blocking vesicular GABA release from either SACs or VIP ACs did not alter dendritic or somatic receptor distributions on the ooDSGCs, showing that neither SAC nor VIP AC GABA release alone is required for the development of inhibitory synapses in ooDSGCs. Furthermore, a reduction in net GABAergic transmission, but not a selective reduction from SACs, increased excitatory drive onto ooDSGCs. This increased excitation may drive a homeostatic increase in ooDSGC somatic GABAA receptors. Differential regulation of GABAA receptors on the ooDSGC’s soma and dendrites could facilitate homeostatic control of the ooDSGC’s output while enabling the assembly of the GABAergic connectivity underlying direction selectivity to be indifferent to altered transmission.

scholarly journals Neural selectivity for visual motion in macaque area V3A

2020 ◽  
Author(s):  
Nardin Nakhla ◽  
Yavar Korkian ◽  
Matthew R. Krause ◽  
Christopher C. Pack
Keyword(s):  
Visual Cortex ◽  
Optic Flow ◽  
Functional Role ◽  
Visual Motion ◽  
Flow Patterns ◽  
Brain Regions ◽  
Direction Selectivity ◽  
Motion Processing ◽  
Imaging Studies ◽  
Motion Direction

AbstractThe processing of visual motion is carried out by dedicated pathways in the primate brain. These pathways originate with populations of direction-selective neurons in the primary visual cortex, which project to dorsal structures like the middle temporal (MT) and medial superior temporal (MST) areas. Anatomical and imaging studies have suggested that area V3A might also be specialized for motion processing, but there have been very few studies of single-neuron direction selectivity in this area. We have therefore performed electrophysiological recordings from V3A neurons in two macaque monkeys (one male and one female) and measured responses to a large battery of motion stimuli that includes translation motion, as well as more complex optic flow patterns. For comparison, we simultaneously recorded the responses of MT neurons to the same stimuli. Surprisingly, we find that overall levels of direction selectivity are similar in V3A and MT and moreover that the population of V3A neurons exhibits somewhat greater selectivity for optic flow patterns. These results suggest that V3A should be considered as part of the motion processing machinery of the visual cortex, in both human and non-human primates.Significance statementAlthough area V3A is frequently the target of anatomy and imaging studies, little is known about its functional role in processing visual stimuli. Its contribution to motion processing has been particularly unclear, with different studies yielding different conclusions. We report a detailed study of direction selectivity in V3A. Our results show that single V3A neurons are, on average, as capable of representing motion direction as are neurons in well-known structures like MT. Moreover, we identify a possible specialization for V3A neurons in representing complex optic flow, which has previously been thought to emerge in higher-order brain regions. Thus it appears that V3A is well-suited to a functional role in motion processing.

Retinal ganglion cells projecting to the rabbit accessory optic system

1980 ◽  
Vol 190 (1) ◽  
pp. 49-61 ◽  
Author(s):  
Clyde W. Oyster ◽  
John I. Simpson ◽  
Ellen S. Takahashi ◽  
Robert E. Soodak
Keyword(s):  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Retinal Ganglion ◽  
Optic System ◽  
Accessory Optic System

Abnormally high variability in the uncrossed retinofugal pathway of mice with albino mosaicism

Development ◽  
1987 ◽  
Vol 101 (4) ◽  
pp. 857-867 ◽  
Author(s):  
R.W. Guillery ◽  
G. Jeffery ◽  
B.M. Cattanach
Keyword(s):  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Gene Dosage ◽  
Optic Tract ◽  
High Variability ◽  
Retinal Ganglion ◽  
Rare Occurrence ◽  
Autosome Translocation ◽  
Open Question ◽  
The Relationship

Female mice showing albino mosaicism due to an X-autosome translocation [Is(In7;X)Ct] have been studied in order to investigate the relationship between the distribution of melanin and the formation, early in development, of the abnormally small uncrossed retinofugal pathway characteristically found in all albino mammals. Earlier evidence indicates that cells normally bearing melanin play a role in producing the abnormality. In the mosaic mice, the albino gene is expressed in only about half of the cells due to random X-inactivation and the patches of normal and albino cells are extremely small relative to total retinal size (less than 1/50). We argued that if all the cells that would normally bear melanin play a role in producing the albino abnormality then the mosaic mice would have a pathway abnormality, about half the size of that in the albino mice. If, however, only a small patch of these cells plays a role, as has been proposed in earlier studies, then one would expect the size of the uncrossed pathway to be highly variable in the mosaic mice. The size of the uncrossed pathway was assessed by placing horseradish peroxidase in the region of the optic tract and lateral geniculate nucleus unilaterally and then counting the number of retrogradely labelled retinal ganglion cells on the same side. The mosaic mice showed a highly variable uncrossed pathway. In some of the mosaic mice, it was the same size as in the albinos and, in others, it was the same size as in normally pigmented mice. Surprisingly, in a small number of mosaic mice, the uncrossed pathway was larger than normal. Whether this relatively rare occurrence of a supernormal uncrossed pathway is due to the higher gene dosage or to the translocation itself remains an open question.

Membrane Properties and Monosynaptic Retinal Excitation of Neurons in the Turtle Accessory Optic System

1997 ◽  
Vol 78 (2) ◽  
pp. 614-627 ◽  
Author(s):  
Naoki Kogo ◽  
Michael Ariel
Keyword(s):  
Receptive Field ◽  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Membrane Properties ◽  
Retinal Ganglion ◽  
Optic System ◽  
Accessory Optic System ◽  
Postsynaptic Potentials ◽  
Synaptic Inputs ◽  
Bon Cells

Kogo, Naoki and Michael Ariel. Membrane properties and monosynaptic retinal excitation of neurons in the turtle accessory optic system. J. Neurophysiol. 78: 614–627, 1997. Using an eye-attached isolated brain stem preparation of a turtle, Pseudemys scripta elegans, in conjunction with whole cell patch techniques, we recorded intracellular activity of accessory optic system neurons in the basal optic nucleus (BON). This technique offered long-lasting stable recordings of individual synaptic events. In the reduced preparation (most of the dorsal structures were removed), large spontaneous excitatory synaptic inputs [excitatory postsynaptic potentials (EPSPs)] were frequently recorded. Spontaneous inhibitory postsynaptic potentials were rarely observed except in few cases. Most EPSPs disappeared after injection of lidocaine into the retina. A few EPSPs of small size remained, suggesting that these EPSPs either were from intracranial sources or may have been miniature spontaneous synaptic potentials from retinal ganglion cell axon terminals. Population EPSPs were synchronously evoked by electrical stimulation of the contralateral optic nerve. Their constant onset latency and their ability to follow short-interval paired stimulation indicated that much of the population EPSP's response was monosynaptic. Visually evoked BON spikes and EPSP inputs to BON showed direction sensitivity when a moving pattern was projected onto the entire contralateral retina. With the use of smaller moving patterns, the receptive field of an individual BON cell was identified. A small spot of light, projected within the receptive field, guided the placement of a bipolar stimulation electrode to activate retinal ganglion cells that provided input to that BON cell. EPSPs evoked by this retinal microstimulation showed features of unitary EPSPs. Those EPSPs had distinct low current thresholds. Recruitment of other inputs was only evident when the stimulation level was increased substantially above threshold. The average size of evoked unitary EPSPs was 7.8 mV, confirming the large size of synaptic inputs of this system relative to nonsynaptic noise. EPSP shape was plotted (rise time vs. amplitude), with the use of either evoked unitary EPSPs or spontaneous EPSPs. Unlike samples of spontaneous EPSPs, data from many unitary EPSPs formed distinct clusters in these scatterplots, indicating that these EPSPs had a unique shape among the whole population of EPSPs. In most BON cells studied, hyperpolarization-activated channels caused a slow depolarization sag that reached a plateau within 0.5–1 s. This property suggests that BON cells may be more complicated than a simple site for convergence of direction-sensitive retinal ganglion cells to form a central retinal slip signal for control of oculomotor reflexes.

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