scholarly journals A retinal circuit that vetoes optokinetic responses to fast visual motion

2021 ◽  
Author(s):  
Adam Mani ◽  
Xinzhu Yang ◽  
Tiffany Zhao ◽  
David M Berson
Keyword(s):  
Retinal Image ◽  
Visual Motion ◽  
Amacrine Cells ◽  
Image Motion ◽  
Mouse Retina ◽  
Specific Class ◽  
Global Motion ◽  
Optokinetic Responses ◽  
Fast Motion ◽  
Glycinergic Inhibition

Optokinetic nystagmus (OKN) is a visuomotor reflex that works in tandem with the vestibulo-ocular reflex (VOR) to stabilize the retinal image during self-motion. OKN requires information about both the direction and speed of retinal image motion. Both components are computed within the retina because they are already encoded in the spike trains of the specific class of retinal output neurons that drives OKN ─ the ON direction-selective ganglion cells (ON DSGCs). The synaptic circuits that shape the directional tuning of ON DSGCs, anchored by starburst amacrine cells, are largely established. By contrast, little is known about the cells and circuits that account for the slow speed preference of ON DSGCs and, thus, of OKN that they drive. A recent study in rabbit retina implicates feedforward glycinergic inhibition as the key suppressor of ON DSGC responses to fast motion. Here, we used serial-section electron microscopy, patch recording, pharmacology, and optogenetic and chemogenetic manipulations to probe this circuit in mouse retina. We confirm a central role for feedforward glycinergic inhibition onto ON DSGCs and identify a surprising primary source for this inhibition ─ the VGluT3 amacrine cell (VG3 cell). VG3 cells are retinal interneurons that release both glycine and glutamate, exciting some neurons and inhibiting others. Their role in suppressing the response of ON DSGCs to rapid global motion is surprising. VG3 cells had been thought to provide glutamatergic excitation to ON-DSGCs, not glycinergic inhibition, and because they have strong receptive fields surrounds which might have been expected to render them unresponsive to global motion. In fact, VG3 cells are robustly activated by the sorts of fast global motion that suppress ON DSGCs and weaken optokinetic responses as revealed by dendritic Ca+2 imaging, since surround suppression is less prominent when probed with moving gratings than with spots. VG3 cells excite many ganglion cell types through their release of glutatmate. We confirmed that for one such type, the ON-OFF DSGCs, VG3 cells enhance the response to fast motion in these cells, just as they suppress it in ON DSGCs. Together, our results assign a novel function to VGluT3 cells in shaping the velocity range over which retinal slip drives compensatory image stabilizing eye movements. In addition, fast speed motion signal from VGluT3 cells is used by ON-OFF DSGCs to extend the speed range over which they respond, and might be used to shape the speed tuning or temporal bandwidth of the responses of other RGCs.

scholarly journals Local processing in neurites of VGluT3-expressing amacrine cells differentially organizes visual information

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jen-Chun Hsiang ◽  
Keith P Johnson ◽  
Linda Madisen ◽  
Hongkui Zeng ◽  
Daniel Kerschensteiner
Keyword(s):  
Visual Processing ◽  
Visual Information ◽  
Receptive Fields ◽  
Visual Space ◽  
Amacrine Cells ◽  
Object Motion ◽  
Image Motion ◽  
Local Processing ◽  
Mouse Retina ◽  
Population Activity

Neurons receive synaptic inputs on extensive neurite arbors. How information is organized across arbors and how local processing in neurites contributes to circuit function is mostly unknown. Here, we used two-photon Ca2+ imaging to study visual processing in VGluT3-expressing amacrine cells (VG3-ACs) in the mouse retina. Contrast preferences (ON vs. OFF) varied across VG3-AC arbors depending on the laminar position of neurites, with ON responses preferring larger stimuli than OFF responses. Although arbors of neighboring cells overlap extensively, imaging population activity revealed continuous topographic maps of visual space in the VG3-AC plexus. All VG3-AC neurites responded strongly to object motion, but remained silent during global image motion. Thus, VG3-AC arbors limit vertical and lateral integration of contrast and location information, respectively. We propose that this local processing enables the dense VG3-AC plexus to contribute precise object motion signals to diverse targets without distorting target-specific contrast preferences and spatial receptive fields.

Avian vestibuloocular reflex: adaptive plasticity and developmental changes

1982 ◽  
Vol 48 (4) ◽  
pp. 952-967 ◽  
Author(s):  
J. Wallman ◽  
J. Velez ◽  
B. Weinstein ◽  
A. E. Green
Keyword(s):  
Retinal Image ◽  
Visual Motion ◽  
Reversed Phase ◽  
Phase Changes ◽  
Adaptive Plasticity ◽  
Vestibuloocular Reflex ◽  
En Bloc ◽  
Retinal Slip ◽  
Phase Lead ◽  
Optokinetic Responses

1. This study demonstrates plasticity of the vestibuloocular reflex (VOR) in chickens and compares it to that of other species and to that of newly hatched chicks. Adaptive changes in the VOR were induced by subjecting the animals to combinations of visual and vestibular stimuli that simulated the effect of the VOR being either too low in gain or reversed in phase. 2. The VOR of chickens resembles that of mammals, but the curve of phase lead versus frequency seems shifted toward higher frequencies. The VOR of newly hatched chicks has extremely low gain (less than 0.1). 3. In both the older and newly hatched animals, the VOR gain increased substantially after 2 h in an environment in which the imposed en bloc rotations produced increased retinal image slip in the normal directions. Similarly, 2 h of reversed retinal image slip produced decreased VOR gain and, in some cases, reversal fo the phase of the VOR. The gain changes were largest at the "training" frequency. The phase changes were in the direction of increased phase lead. Changes in the gains of the optokinetic responses and of the combination of VOR and optokinetic responses were also seen, especially in the newly hatched animals. 4. The newly hatched birds showed the largest VOR changes in the increased-gain situation, whereas the older birds showed the largest changes in the reversed-phase situation, as assessed by the changes in the average retinal slip velocity experienced. These results may well not be a consequence of differences in age, per se, but of differences in average retinal slip experienced in the two experimental situations at the start of the trial because of the lower VOR gain of the newly hatched animals. There seems to be no dramatic difference in VOR plasticity between newly hatched and older birds. 5. Our results with reversed visual motion are substantially different from those obtained in similar studies on rabbits, suggesting that these two species use different error signals to control the adaptive adjustment of the VOR.

Direction and speed tuning to visual motion in cortical areas MT and MSTd during smooth pursuit eye movements

2011 ◽  
Vol 105 (4) ◽  
pp. 1531-1545 ◽  
Author(s):  
Naoko Inaba ◽  
Kenichiro Miura ◽  
Kenji Kawano
Keyword(s):  
Eye Movements ◽  
Retinal Image ◽  
Visual Motion ◽  
Natural World ◽  
Image Motion ◽  
Large Field ◽  
Moving Target ◽  
Cortical Areas ◽  
Retinal Image Motion ◽  
Background Motion

When tracking a moving target in the natural world with pursuit eye movement, our visual system must compensate for the self-induced retinal slip of the visual features in the background to enable us to perceive their actual motion. We previously reported that the speed of the background stimulus in space is represented by dorsal medial superior temporal (MSTd) neurons in the monkey cortex, which compensate for retinal image motion resulting from eye movements when the direction of the pursuit and background motion are parallel to the preferred direction of each neuron. To further characterize the compensation observed in the MSTd responses to the background motion, we recorded single unit activities in cortical areas middle temporal (MT) and MSTd, and we selected neurons responsive to a large-field visual stimulus. We studied their responses to the large-field stimulus in the background while monkeys pursued a moving target and while fixated a stationary target. We investigated whether compensation for retinal image motion of the background depended on the speed of pursuit. We also asked whether the directional selectivity of each neuron in relation to the external world remained the same even during pursuit and whether compensation for retinal image motion occurred irrespective of the direction of the pursuit. We found that the majority of the MSTd neurons responded to the visual motion in space by compensating for the image motion on the retina resulting from the pursuit regardless of pursuit speed and direction, whereas most of the MT neurons responded in relation to the genuine retinal image motion.

scholarly journals Modulation of Visual Signals in Macaque MT and MST Neurons During Pursuit Eye Movement

2009 ◽  
Vol 102 (6) ◽  
pp. 3225-3233 ◽  
Author(s):  
Leanne Chukoskie ◽  
J. Anthony Movshon
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Retinal Image ◽  
Visual Motion ◽  
Single Cells ◽  
Response Amplitude ◽  
Visual Signals ◽  
Image Motion ◽  
Visual Responses ◽  
Retinal Image Motion

Retinal image motion is produced with each eye movement, yet we usually do not perceive this self-produced “reafferent” motion, nor are motion judgments much impaired when the eyes move. To understand the neural mechanisms involved in processing reafferent motion and distinguishing it from the motion of objects in the world, we studied the visual responses of single cells in middle temporal (MT) and medial superior temporal (MST) areas during steady fixation and smooth-pursuit eye movements in awake, behaving macaques. We measured neuronal responses to random-dot patterns moving at different speeds in a stimulus window that moved with the pursuit target and the eyes. This allowed us to control retinal image motion at all eye velocities. We found the expected high proportion of cells selective for the direction of visual motion. Pursuit tracking changed both response amplitude and preferred retinal speed for some cells. The changes in preferred speed were on average weakly but systematically related to the speed of pursuit for area MST cells, as would be expected if the shifts in speed selectivity were compensating for reafferent input. In area MT, speed tuning did not change systematically during pursuit. Many cells in both areas also changed response amplitude during pursuit; the most common form of modulation was response suppression when pursuit was opposite in direction to the cell's preferred direction. These results suggest that some cells in area MST encode retinal image motion veridically during eye movements, whereas others in both MT and MST contribute to the suppression of visual responses to reafferent motion.

Modulation by Zn2+ of GABA responses in bipolar cells of the mouse retina

2000 ◽  
Vol 17 (2) ◽  
pp. 273-281 ◽  
Author(s):  
M. KANEDA ◽  
B. ANDRÁSFALVY ◽  
A. KANEKO
Keyword(s):  
Axon Terminal ◽  
Inhibitory Action ◽  
Phosphinic Acid ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Induced Responses ◽  
Inhibitory Interaction ◽  
Cell Recording ◽  
Recording Conditions

The localization of endogenous Zn2+ in the mouse retina was examined histochemically and the inhibitory action of Zn2+ on GABA-induced responses was studied in bipolar cells isolated from the mouse retina. Accumulation of endogenous Zn2+ was detected in photoreceptors, bipolar, and/or amacrine cells by either the bromopyridylazo-diethylaminophenol method or the dithizone method. Under whole-cell recording conditions, GABA induced a Cl− current in isolated bipolar cells. The current consisted of two components. The first component was inhibited completely by application of 100 μM bicuculline, suggesting that this is a GABAA-receptor mediated current. The second component was inhibited completely by 100 μM 3-aminopropyl-(methyl)-phosphinic acid, suggesting that this is a GABAC-receptor mediated current. GABAC receptors were present at a higher density on the axon terminal than on dendrites. Zn2+ inhibited both GABAA and GABAC receptors. GABAC receptors were more susceptible to Zn2+; the IC50 for the GABAA receptor was 67.4 μM and that for the GABAC receptor was 1.9 μM. These results suggest that Zn2+ modulates the inhibitory interaction between amacrine and bipolar cells, particularly that mediated by the GABAC receptor.

Amacrine-to-amacrine cell inhibition: Spatiotemporal properties of GABA and glycine pathways

2011 ◽  
Vol 28 (3) ◽  
pp. 193-204 ◽  
Author(s):  
XIN CHEN ◽  
HAIN ANN HSUEH ◽  
FRANK S. WERBLIN
Keyword(s):  
Amacrine Cell ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Peak Level ◽  
Wide Field ◽  
Gabaergic Inhibition ◽  
Onset Latency ◽  
Temporal Properties ◽  
Glycinergic Inhibition ◽  
Cell Inhibition

AbstractWe measured the spatial and temporal properties of GABAergic and glycinergic inhibition to amacrine cells in the whole-mount rabbit retina. The amacrine cells were parsed into two morphological classes: narrow-field cells with processes spreading less than 200 μm and wide-field cells with processes extending more than 300 μm. The inhibition was also parsed into two types: sustained glycine and transient GABA. Narrow-field amacrine cells receive 1) very transient GABAergic inhibition with a fast onset latency of 140 ± 16 ms decaying to 30% of the peak level within 208 ± 27 ms elicited broadly over a lateral distance of up to 1500 μm and 2) sustained glycinergic inhibition with a medium onset latency of 286 ± 23 ms that was elicited over a spatial area often broader than the processes of the narrow-field amacrine cells. Wide-field amacrine cells received sustained glycinergic inhibition but no broad transient GABAergic inhibition. Surprisingly, neither of these amacrine cell classes received sustained local GABAergic inhibition, commonly found in an earlier study of ganglion cells.

Retinal Image Motion During Deliberate Fixation

2000 ◽  
Vol 78 (2) ◽  
pp. 131-142 ◽  
Author(s):  
James W. Ness ◽  
Harry Zwick ◽  
Bruce E. Stuck ◽  
David J. Lurid ◽  
Brian J. Lurid ◽  
...  
Keyword(s):  
Retinal Image ◽  
Image Motion ◽  
Retinal Image Motion
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