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.

scholarly journals Intrinsic properties and functional circuitry of the AII amacrine cell

2012 ◽  
Vol 29 (1) ◽  
pp. 51-60 ◽  
Author(s):  
JONATHAN B. DEMB ◽  
JOSHUA H. SINGER
Keyword(s):  
Visual Processing ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Retinal Neuron ◽  
Motion Sensitivity ◽  
Network Properties ◽  
Aii Amacrine

AbstractAmacrine cells represent the most diverse class of retinal neuron, comprising dozens of distinct cell types. Each type exhibits a unique morphology and generates specific visual computations through its synapses with a subset of excitatory interneurons (bipolar cells), other amacrine cells, and output neurons (ganglion cells). Here, we review the intrinsic and network properties that underlie the function of the most common amacrine cell in the mammalian retina, the AII amacrine cell. The AII connects rod and cone photoreceptor pathways, forming an essential link in the circuit for rod-mediated (scotopic) vision. As such, the AII has become known as the rod–amacrine cell. We, however, now understand that AII function extends to cone-mediated (photopic) vision, and AII function in scotopic and photopic conditions utilizes the same underlying circuit: AIIs are electrically coupled to each other and to the terminals of some types of ON cone bipolar cells. The direction of signal flow, however, varies with illumination. Under photopic conditions, the AII network constitutes a crossover inhibition pathway that allows ON signals to inhibit OFF ganglion cells and contributes to motion sensitivity in certain ganglion cell types. We discuss how the AII’s combination of intrinsic and network properties accounts for its unique role in visual processing.

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 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.

Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina

1997 ◽  
Vol 14 (3) ◽  
pp. 507-522 ◽  
Author(s):  
Donna K. Stafford ◽  
Dennis M. Dacey
Keyword(s):  
Receptive Field ◽  
Amacrine Cell ◽  
Dendritic Tree ◽  
Amacrine Cells ◽  
Cell Types ◽  
Macaque Monkey ◽  
Cell Type ◽  
Slow Potential ◽  
Spike Discharge

AbstractWe characterized the light response, morphology, and receptive-field structure of a distinctive amacrine cell type (Dacey, 1989), termed here the Al amacrine, by applying intracellular recording and staining methods to the macaque monkey retina in vitro. A1 cells show two morphologically distinct components: a highly branched and spiny dendritic tree, and a more sparsely branched axon-like tree that arises from one or more hillock-like structures near the soma and extends for several millimeters beyond the dendritic tree. Intracellular injection of Neurobiotin reveals an extensive and complex pattern of tracer coupling to neighboring A1 amacrine cells, to two other amacrine cell types, and to a single ganglion cell type. The A1 amacrine is an ON-OFF cell, showing a large (10–20 mV) transient depolarization at both onset and offset of a photopic, luminance modulated stimulus. A burst of fast, large-amplitude (Σ60 mV) action potentials is associated with the depolarizations at both the ON and OFF phase of the response. No evidence was found for an inhibitory receptive-field surround. The spatial extent of the ON-OFF response was mapped by measuring the strength of the spike discharge and/or the amplitude of the depolarizing slow potential as a function of the position of a bar or spot of light within the receptive field. Receptive fields derived from the slow potential and associated spike discharge corresponded in size and shape. Thus, the amplitude of the slow potential above spike threshold was well encoded as spike frequency. The diameter of the receptive field determined from the spike discharge was Σ10% larger than the spiny dendritic field. The correspondence in size between the spiking receptive field and the spiny dendritic tree suggests that light driven signals are conducted to the soma from the dendritic tree but not from the axon-like arbor. The function of the axon-like component is unknown but we speculate that it serves a classical output function, transmitting spikes distally from initiation sites near the soma.

scholarly journals Center-surround interactions underlie bipolar cell motion sensing in the mouse retina

2021 ◽  
Author(s):  
Sarah Strauss ◽  
Maria M Korympidou ◽  
Yanli Ran ◽  
Katrin Franke ◽  
Timm Schubert ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Motion Processing ◽  
Local Motion ◽  
Motion Sensing ◽  
Motion Sensitivity

Motion is a critical aspect of vision. We studied the representation of motion in mouse retinal bipolar cells and found, surprisingly, that some bipolar cells possess motion-sensing capabilities that rely on their center-surround receptive fields. Using a glutamate sensor, we directly observed motion-sensitive bipolar cell synaptic output, which was strongest for local motion and dependent on the motion's origin. We characterized bipolar cell receptive fields and found that there are motion and non-motion sensitive bipolar cell types, the majority being motion sensitive. Next, we used these bipolar cell receptive fields along with connectomics to design biophysical models of downstream cells. The models and experiments demonstrated that bipolar cells pass motion-sensitive excitation to starburst amacrine cells through direction-specific signals mediated by bipolar cells' center-surround receptive field structure. As bipolar cells provide excitation to most amacrine and ganglion cells, their motion sensitivity may contribute to motion processing throughout the visual system.

Direction selectivity in a model of the starburst amacrine cell

2004 ◽  
Vol 21 (4) ◽  
pp. 611-625 ◽  
Author(s):  
JOHN J. TUKKER ◽  
W. ROWLAND TAYLOR ◽  
ROBERT G. SMITH
Keyword(s):  
Amacrine Cell ◽  
Dendritic Tree ◽  
Sine Wave ◽  
Direction Selectivity ◽  
Membrane Properties ◽  
Calcium Signal ◽  
Inhibitory Input ◽  
Excitatory Postsynaptic Potential ◽  
Global Signal ◽  
Starburst Amacrine Cell

The starburst amacrine cell (SBAC), found in all mammalian retinas, is thought to provide the directional inhibitory input recorded in On–Off direction-selective ganglion cells (DSGCs). While voltage recordings from the somas of SBACs have not shown robust direction selectivity (DS), the dendritic tips of these cells display direction-selective calcium signals, even when γ-aminobutyric acid (GABAa,c) channels are blocked, implying that inhibition is not necessary to generate DS. This suggested that the distinctive morphology of the SBAC could generate a DS signal at the dendritic tips, where most of its synaptic output is located. To explore this possibility, we constructed a compartmental model incorporating realistic morphological structure, passive membrane properties, and excitatory inputs. We found robust DS at the dendritic tips but not at the soma. Two-spot apparent motion and annulus radial motion produced weak DS, but thin bars produced robust DS. For these stimuli, DS was caused by the interaction of a local synaptic input signal with a temporally delayed “global” signal, that is, an excitatory postsynaptic potential (EPSP) that spread from the activated inputs into the soma and throughout the dendritic tree. In the preferred direction the signals in the dendritic tips coincided, allowing summation, whereas in the null direction the local signal preceded the global signal, preventing summation. Sine-wave grating stimuli produced the greatest amount of DS, especially at high velocities and low spatial frequencies. The sine-wave DS responses could be accounted for by a simple mathematical model, which summed phase-shifted signals from soma and dendritic tip. By testing different artificial morphologies, we discovered DS was relatively independent of the morphological details, but depended on having a sufficient number of inputs at the distal tips and a limited electrotonic isolation. Adding voltage-gated calcium channels to the model showed that their threshold effect can amplify DS in the intracellular calcium signal.

scholarly journals Computational and Molecular Properties of Starburst Amacrine Cell Synapses Differ With Postsynaptic Cell Type

2021 ◽  
Vol 15 ◽  
Author(s):  
Joseph Pottackal ◽  
Joshua H. Singer ◽  
Jonathan B. Demb
Keyword(s):  
Amacrine Cell ◽  
Ganglion Cells ◽  
Spatial Scales ◽  
Cell Types ◽  
Inhibitory Synapses ◽  
Mouse Retina ◽  
Presynaptic Neuron ◽  
Postsynaptic Cell ◽  
Low Pass ◽  
Starburst Amacrine Cell

A presynaptic neuron can increase its computational capacity by transmitting functionally distinct signals to each of its postsynaptic cell types. To determine whether such computational specialization occurs over fine spatial scales within a neurite arbor, we investigated computation at output synapses of the starburst amacrine cell (SAC), a critical component of the classical direction-selective (DS) circuit in the retina. The SAC is a non-spiking interneuron that co-releases GABA and acetylcholine and forms closely spaced (<5 μm) inhibitory synapses onto two postsynaptic cell types: DS ganglion cells (DSGCs) and neighboring SACs. During dynamic optogenetic stimulation of SACs in mouse retina, whole-cell recordings of inhibitory postsynaptic currents revealed that GABAergic synapses onto DSGCs exhibit stronger low-pass filtering than those onto neighboring SACs. Computational analyses suggest that this filtering difference can be explained primarily by presynaptic properties, rather than those of the postsynaptic cells per se. Consistent with functionally diverse SAC presynapses, blockade of N-type voltage-gated calcium channels abolished GABAergic currents in SACs but only moderately reduced GABAergic and cholinergic currents in DSGCs. These results jointly demonstrate how specialization of synaptic outputs could enhance parallel processing in a compact interneuron over fine spatial scales. Moreover, the distinct transmission kinetics of GABAergic SAC synapses are poised to support the functional diversity of inhibition within DS circuitry.

Computation of motion direction in the vertebrate retina

e-Neuroforum ◽  
2012 ◽  
Vol 18 (3) ◽  
Author(s):  
T. Euler ◽  
S.E. Hausselt
Keyword(s):  
Large Scale ◽  
Petri Dish ◽  
Cell Types ◽  
Direction Selectivity ◽  
Dendritic Morphology ◽  
Image Motion ◽  
Target Area ◽  
Motion Direction ◽  
Preferred Direction ◽  
The Brain

AbstractHow direction of image motion is detected as early as at the level of the vertebrate eye has been intensively studied in retina research. Although the first direction-selective (DS) ret­inal ganglion cells were already described in the 1960s and have since then been in the fo­cus of many studies, scientists are still puz­zled by the intricacy of the neuronal circuits and computational mechanisms underlying retinal direction selectivity. The fact that the retina can be easily isolated and studied in a Petri dish-by presenting light stimuli while recording from the various cell types in the retinal circuits-in combination with the ex­tensive anatomical, molecular and physiolog­ical knowledge about this part of the brain presents a unique opportunity for studying this intriguing visual circuit in detail. This ar­ticle provides a brief overview of the histo­ry of research on retinal direction selectivi­ty, but then focuses on the past decade and the progress achieved, in particular driven by methodological advances in optical record­ing techniques, molecular genetics approach­es and large-scale ultrastructural reconstruc­tions. As it turns out, retinal direction selec­tivity is a complex, multi-tiered computation, involving dendrite-intrinsic mechanisms as well as several types of network interactions on the basis of highly selective, likely genet­ically predetermined synaptic connectivi­ty. Moreover, DS ganglion cell types appear to be more diverse than previously thought, differing not only in their preferred direction and response polarity, but also in physiology, DS mechanism, dendritic morphology and, importantly, the target area of their projec­tions in the brain.

Rod signals are routed through specific Off cone bipolar cells in primate retina

2020 ◽  
Author(s):  
Amanda J. McLaughlin ◽  
Kumiko A. Percival ◽  
Jacqueline Gayet-Primo ◽  
Teresa Puthussery
Keyword(s):  
Bipolar Cell ◽  
Amacrine Cell ◽  
Amacrine Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Visual Signals ◽  
Night Time ◽  
Pass Through ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

AbstractAdapting between scotopic and photopic illumination involves switching the routing of retinal signals between rod and cone-dominated circuits. In the daytime, cone signals pass through parallel On and Off cone bipolar cells, that are sensitive to increments and decrements in luminance, respectively. At night, rod signals are routed into these cone-pathways via a key glycinergic interneuron, the AII amacrine cell (AII-AC). In primates, it is not known whether AII-ACs contact all Off-bipolar cell types indiscriminately, or whether their outputs are biased towards specific Off-bipolar cell types. Here, we show that the rod-driven glycinergic output of AII-ACs is strongly biased towards a subset of macaque Off-cone bipolar cells. The Off-bipolar types that receive this glycinergic input have sustained physiological properties and include the Off-midget bipolar cells, which provide excitatory input to the Off-midget ganglion cells (parvocellular pathway). The kinetics of the glycinergic events are consistent with the involvement of the α1 glycine receptor subunit. Taken together with results in mouse retina, our findings point towards a conserved motif whereby rod signals are preferentially routed into sustained Off signaling pathways.Significance StatementVisual signals pass through different retinal neurons depending on the prevailing level of illumination. Under night-time light levels, signals from rods pass through the AII amacrine cell, an inhibitory interneuron that routes rod signals into On and Off bipolar cells to detect increments and decrements in light intensity, respectively. Here, we show in primate retina that the output of AII amacrine cells is strongly biased towards specific Off bipolar cell types, which suggests that rod signals reach the brain via specific neural channels. Our results further our understanding of how visual signals are routed through visual circuits during night-time vision.

scholarly journals Cell density ratios in a foveal patch in macaque retina

2003 ◽  
Vol 20 (2) ◽  
pp. 189-209 ◽  
Author(s):  
KAREEM M. AHMAD ◽  
KARL KLUG ◽  
STEVE HERR ◽  
PETER STERLING ◽  
STAN SCHEIN
Keyword(s):  
Cell Density ◽  
Bipolar Cell ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Horizontal Cell ◽  
Macaque Monkey ◽  
Bipolar Cells ◽  
Thin Sections ◽  
Density Ratios ◽  
Cone Bipolar Cells

We examine the assumptions that the fovea contains equal numbers of inner (invaginating or ON) and outer (flat or OFF) midget bipolar cells and equal numbers of inner and outer diffuse bipolar cells. Based on reconstruction from electron photomicrographs of serial thin sections through the fovea of a macaque monkey, we reject both assumptions. First, every foveal L and M cone is presynaptic to one inner and one outer midget bipolar cell; however, S cones are presynaptic to one outer but no inner midget bipolar cell. Second, we measure the density of all foveal cells in the same patch of fovea, affording accurate cell density ratios. For each foveal cone pedicle, at a density of 26,500 mm−2, there is close to one (0.88) outer diffuse bipolar cell but only 0.40 inner diffuse bipolar cells. This asymmetry may be related to differences in resolution and sensitivity for light increments and decrements. We also find one (1.01) Müller cell, one (1.01) amacrine cell in the inner nuclear layer, and close to one (0.83) horizontal cell for each cone pedicle. In addition, for each S cone, there are two inner S-cone bipolar cells and two small bistratified ganglion cells. In total, there are 3.4 cone bipolar cells per cone but only 2.6 ganglion cells per cone. The latter ratio is enough to accommodate one midget ganglion cell for each midget bipolar cell.

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