scholarly journals Synapse-specific direction selectivity in retinal bipolar cell axon terminals

2020 ◽  
Author(s):  
Akihiro Matsumoto ◽  
Weaam Agbariah ◽  
Stella Solveig Nolte ◽  
Rawan Andrawos ◽  
Hadara Levi ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cells ◽  
Visual Pathway ◽  
Direction Selectivity ◽  
Image Motion ◽  
Gabaergic Inhibition ◽  
Axon Terminals ◽  
Two Photon ◽  
Synaptic Release ◽  
Specific Direction

AbstractThe ability to encode the direction of image motion is fundamental to our sense of vision. Direction selectivity along the four cardinal directions is thought to originate in direction-selective ganglion cells (DSGCs), due to directionally-tuned GABAergic suppression by starburst cells. Here, by utilizing two-photon glutamate imaging to measure synaptic release, we reveal that direction selectivity along all four directions arises earlier than expected, at bipolar cell outputs. Thus, DSGCs receive directionally-aligned glutamatergic inputs from bipolar cell boutons. We further show that this bouton-specific tuning relies on cholinergic excitation and GABAergic inhibition from starburst cells. In this way, starburst cells are able to refine directional tuning in the excitatory visual pathway by modulating the activity of DSGC dendrites and their axonal inputs using two different neurotransmitters.

scholarly journals All-optical interrogation of a direction selective retinal circuit by holographic wave front shaping

2019 ◽  
Author(s):  
G.L.B Spampinato ◽  
E. Ronzitti ◽  
V. Zampini ◽  
U. Ferrari ◽  
F. Trapani ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Single Cells ◽  
Direction Selectivity ◽  
Retinal Neurons ◽  
Two Photon ◽  
Light Levels ◽  
All Optical ◽  
Dim Light

AbstractDirection selective (DS) ganglion cells (GC) in the retina maintain their tuning across a broad range of light levels. Yet very different circuits can shape their responses from bright to dim light, and their respective contributions are difficult to tease apart. In particular, the contribution of the rod bipolar cell (RBC) primary pathway, a key player in dim light, is unclear. To understand its contribution to DSGC response, we designed an all-optical approach allowing precise manipulation of single retinal neurons. Our system activates single cells in the bipolar cell (BC) layer by two-photon (2P) temporally focused holographic illumination, while recording the activity in the ganglion cell layer by 2P Ca2 imaging. By doing so, we demonstrate that RBCs provide an asymmetric input to DSGCs, suggesting they contribute to their direction selectivity. Our results suggest that every circuit providing an input to direction selective cells can generate direction selectivity by itself. This hints at a general principle to achieve robust selectivity in sensory areas.

scholarly journals Direction selectivity in retinal bipolar cell axon terminals

Neuron ◽  
2021 ◽  
Author(s):  
Akihiro Matsumoto ◽  
Weaam Agbariah ◽  
Stella Solveig Nolte ◽  
Rawan Andrawos ◽  
Hadara Levi ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Direction Selectivity ◽  
Cell Axon ◽  
Axon Terminals

scholarly journals Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

2014 ◽  
Vol 112 (8) ◽  
pp. 1950-1962 ◽  
Author(s):  
Minggang Chen ◽  
Seunghoon Lee ◽  
Silvia J. H. Park ◽  
Loren L. Looger ◽  
Z. Jimmy Zhou
Keyword(s):  
Receptive Field ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Bipolar Cells ◽  
Visual Signals ◽  
Mouse Retina ◽  
Patch Clamp Recording ◽  
Axon Terminals ◽  
Starburst Amacrine Cells

Retinal bipolar cells (BCs) transmit visual signals in parallel channels from the outer to the inner retina, where they provide glutamatergic inputs to specific networks of amacrine and ganglion cells. Intricate network computation at BC axon terminals has been proposed as a mechanism for complex network computation, such as direction selectivity, but direct knowledge of the receptive field property and the synaptic connectivity of the axon terminals of various BC types is required in order to understand the role of axonal computation by BCs. The present study tested the essential assumptions of the presynaptic model of direction selectivity at axon terminals of three functionally distinct BC types that ramify in the direction-selective strata of the mouse retina. Results from two-photon Ca2+ imaging, optogenetic stimulation, and dual patch-clamp recording demonstrated that 1) CB5 cells do not receive fast GABAergic synaptic feedback from starburst amacrine cells (SACs); 2) light-evoked and spontaneous Ca2+ responses are well coordinated among various local regions of CB5 axon terminals; 3) CB5 axon terminals are not directionally selective; 4) CB5 cells consist of two novel functional subtypes with distinct receptive field structures; 5) CB7 cells provide direct excitatory synaptic inputs to, but receive no direct GABAergic synaptic feedback from, SACs; and 6) CB7 axon terminals are not directionally selective, either. These findings help to simplify models of direction selectivity by ruling out complex computation at BC terminals. They also show that CB5 comprises two functional subclasses of BCs.

scholarly journals The functional organization of excitation and inhibition in the dendrites of mouse direction-selective ganglion cells

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Varsha Jain ◽  
Benjamin L Murphy-Baum ◽  
Geoff deRosenroll ◽  
Santhosh Sethuramanujam ◽  
Mike Delsey ◽  
...  
Keyword(s):  
Functional Organization ◽  
Ganglion Cells ◽  
Direction Selectivity ◽  
Neuronal Function ◽  
Dendritic Trees ◽  
Fine Grained ◽  
Two Photon ◽  
Cell Ablation ◽  
Cell Circuit ◽  
Subcellular Level

Recent studies indicate that the precise timing and location of excitation and inhibition (E/I) within active dendritic trees can significantly impact neuronal function. How synaptic inputs are functionally organized at the subcellular level in intact circuits remains unclear. To address this issue, we took advantage of the retinal direction-selective ganglion cell circuit, where directionally tuned inhibition is known to shape non-directional excitatory signals. We combined two-photon calcium imaging with genetic, pharmacological, and single-cell ablation methods to examine the extent to which inhibition ‘vetoes’ excitation at the level of individual dendrites of direction-selective ganglion cells. We demonstrate that inhibition shapes direction selectivity independently within small dendritic segments (<10µm) with remarkable accuracy. The data suggest that the parallel processing schemes proposed for direction encoding could be more fine-grained than previously envisioned.

scholarly journals Direction selectivity in retinal bipolar cell axon terminals

Neuron ◽  
2021 ◽  
Vol 109 (23) ◽  
pp. 3895-3896
Author(s):  
Akihiro Matsumoto ◽  
Weaam Agbariah ◽  
Stella Solveig Nolte ◽  
Rawan Andrawos ◽  
Hadara Levi ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Direction Selectivity ◽  
Cell Axon ◽  
Axon Terminals

Roles of aspartate and glutamate in synaptic transmission in rabbit retina. II. Inner plexiform layer

1985 ◽  
Vol 53 (3) ◽  
pp. 714-725 ◽  
Author(s):  
S. A. Bloomfield ◽  
J. E. Dowling
Keyword(s):  
Membrane Potential ◽  
Bipolar Cell ◽  
Ganglion Cells ◽  
Plexiform Layer ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Retinal Neurons ◽  
Inner Retina ◽  
Axon Terminals ◽  
Cell Responses

Intracellular recordings were obtained from amacrine and ganglion cells in the superfused, isolated retina-eyecup of the rabbit. The putative neurotransmitters aspartate, glutamate, and several of their analogues were added to the superfusate while the membrane potential and light-responsiveness of the retinal neurons were monitored. Both L-aspartate and L-glutamate displayed excitatory actions on the activity of the vast majority of amacrine and ganglion cells studied. However, these agents occasionally appeared to inhibit the responses of the inner retinal neurons by producing hyperpolarization of the membrane potential and blockage of the light-evoked responses. In either case, the effects of aspartate and glutamate were indistinguishable. The glutamate analogues kainate and quisqualate produced strong excitatory effects on the responses of amacrine and ganglion cells at concentrations some 200-fold less than those needed to obtain similar effects with aspartate or glutamate. The aspartate analogue, n-methyl DL-aspartate (NMDLA), also produced strong excitatory effects but was approximately three times less potent than kainate or quisqualate. On one occasion, we encountered a ganglion cell that was depolarized by kainate, but hyperpolarized by NMDLA. The glutamate antagonist alpha-methyl glutamate and the aspartate antagonist alpha-amino adipate effectively blocked the responses of amacrine and ganglion cells. However, on any one cell, one antagonist was always clearly more potent than the other. We examined the actions of the glutamate analogue 2-amino-4-phosphonobutyrate (APB) on the responses of inner retinal neurons and found that it selectively abolished all "on" activity in the inner retina. Together with our finding that APB selectively abolishes on-bipolar cell responses (see Ref. 6), these data support the hypothesis that on-bipolar cells subserve the "on" activity of amacrine and ganglion cells. Our data suggest that aspartate and glutamate are excitatory transmitters in the inner retina, possibly being released from bipolar cell axon terminals in the inner plexiform layer.

scholarly journals Retinal waves but not visual experience are required for development of retinal direction selectivity maps

2021 ◽  
Author(s):  
Alexandre Tiriac ◽  
Karina Bistrong ◽  
Marla Feller
Keyword(s):  
Calcium Imaging ◽  
Visual Experience ◽  
Ganglion Cells ◽  
Vertical Component ◽  
Direction Selectivity ◽  
The Body ◽  
Retinal Ganglion ◽  
Retinal Waves ◽  
Two Photon ◽  
Eye Opening

Retinal waves and visual experience have been implicated in the formation of retinotopic and eye-specific maps throughout the visual system, but whether either play a role in the development of the maps within the retina itself is unknown. We explore this question using direction-selective retinal ganglion cells, which are organized into a map that aligns to the body and gravitational axes of optic flow. Using two-photon population calcium imaging, we find that the direction selectivity map is present at eye opening and is unaltered by dark-rearing. Remarkably, the horizontal component of the direction selectivity map is absent in mice lacking normal retinal waves, whereas the vertical component remains normal. These results indicate that intrinsic patterns of activity, rather than extrinsic motion signals are critical for the establishment of direction selectivity maps in the retina.

scholarly journals Activation of the Tonic GABAC Receptor Current in Retinal Bipolar Cell Terminals by Nonvesicular GABA Release

2009 ◽  
Vol 102 (2) ◽  
pp. 691-699 ◽  
Author(s):  
S. M. Jones ◽  
M. J. Palmer
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cells ◽  
Gaba Release ◽  
Visual Signal ◽  
Inhibitory Input ◽  
Axon Terminals ◽  
Gaba Transporters ◽  
Concanamycin A ◽  
Vesicular Release ◽  
Tonic Current

Within the second synaptic layer of the retina, bipolar cell (BC) output to ganglion cells is regulated by inhibitory input to BC axon terminals. GABAA receptors (GABAARs) mediate rapid synaptic currents in BC terminals, whereas GABAC receptors (GABACRs) mediate slow evoked currents and a tonic current, which is strongly regulated by GAT-1 GABA transporters. We have used voltage-clamp recordings from BC terminals in goldfish retinal slices to determine the source of GABA for activation of these currents. Inhibition of vesicular release with concanamycin A or tetanus toxin significantly inhibited GABAAR inhibitory postsynaptic currents and glutamate-evoked GABAAR and GABACR currents but did not reduce the tonic GABACR current, which was also not dependent on extracellular Ca2+. The tonic current was strongly potentiated by inhibition of GABA transaminase, under both normal and Ca2+-free conditions, and was activated by exogenous taurine; however inhibition of taurine transport had little effect. The tonic current was unaffected by GAT-2/3 inhibition and was potentiated by GAT-1 inhibition even in the absence of vesicular release, indicating that it is unlikely to be evoked by reversal of GABA transporters or by ambient GABA. In addition, GABA release does not appear to occur via hemichannels or P2X7 receptors. BC terminals therefore exhibit two forms of GABACR-mediated inhibition, activated by vesicular and by nonvesicular GABA release, which are likely to have distinct functions in visual signal processing. The tonic GABACR current in BC terminals exhibits similar properties to tonic GABAAR and glutamate receptor currents in the brain.

Organization of the primate retina: Light microscopy, with an appendix: A second type of midget bipolar cell in the primate retina

1969 ◽  
Vol 255 (799) ◽  
pp. 109-184 ◽  
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Ganglion Cells ◽  
Horizontal Cell ◽  
Light And Electron Microscopy ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Cell Types ◽  
Inner Plexiform Layer ◽  
Axon Terminals

The structure of the human, but mainly of the rhesus monkey, retina as examined by Golgi-staining techniques is described and interpreted on evidence from both light and electron microscopy. One type of rod bipolar cell and two types of cone bipolar cell are recognized. The rod bipolar is exclusively connected to rods. The midget bipolar is postsynaptic to only one cone but each cone is also presynaptic to a diffuse cone (flat) bipolar. Such flat bipolar cells are in synaptic relationship with about seven cones. No other bipolar cell types have been found. The brush bipolar of Polyak is interpreted as probably a distorted rod bipolar, while Polyak’s centrifugal bipolar is a misinterpretation of the morphology of diffuse amacrine cells. When presumptive centrifugal bipolars were observed they appeared to be a developmental stage of amacrine cells. In the outer plexiform layer two types of horizontal cell have been defined. Each type of horizontal cell has a single axon and two kinds of horizontal cell axon terminals are recognized. In the inner plexiform layer there are two main classes of amacrine cells: the stratified amacrines and the diffuse amacrines. Each class of amacrine has a wide variety of shapes. Polyak’s midget ganglion cell is confirmed and his five other kinds of ganglion cell are classified into diffuse and stratified ganglion cells according to the level at which their dendrites branch within the inner plexiform layer. A fuller summary is given by the diagram and in the legend of figure 98, p. 174. A new type of midget bipolar is described in the Appendix (p. 177).

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