Tracer coupling among regenerated amacrine cells in the retina of the goldfish

AbstractThis study sought to characterize the tracer coupling of regenerated amacrine cells in the retina of the goldfish and assess the integration of regenerated neurons into existing retinal circuits. Regeneration of new neurons from injury-induced progenitors was stimulated by surgically excising a small rectangular piece of retina. Several months after regeneration was complete, intracellular injections of Neurobiotin, a gap junction-permeant tracer, were made into single regenerated amacrine cells or nonregenerated (extant) amacrine cells lying outside the regenerated patch. Two groups of amacrine cells were injected: those that in normal retina are tracer coupled and a single type (the radiate amacrine cell) that is not. The data show that regenerated amacrine cells are tracer coupled to each other and to their homologous counterparts outside the patch of regenerated retina. Regenerated radiate cells possess morphologically abnormal dendrites, but these processes can extend out of regenerated retina into surrounding normal retina. Similarly, the dendrites of extant radiate cells, severed by the original lesion, can regenerate into the patch of regenerated retina. These results indicate that in the goldfish retina the cell-specific junctional circuitry present in normal retina is re-created in the regenerated retina, and suggest that regenerated neurons are functionally integrated into the existing retina.

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Horizontal-cell gap junction in the goldfish retina: area and density of particles as revealed by complementary freeze replicas.

Archives of Histology and Cytology ◽

10.1679/aohc.54.181 ◽

1991 ◽

Vol 54 (2) ◽

pp. 181-188 ◽

Cited By ~ 1

Author(s):

Hiroshi WASHIOKA ◽

Hiroshi WATANABE ◽

Koroku NEGISHI ◽

Akira TONOSAKI

Keyword(s):

Gap Junction ◽

Horizontal Cell ◽

Goldfish Retina

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Calcium From Internal Stores Triggers GABA Release From Retinal Amacrine Cells

Journal of Neurophysiology ◽

10.1152/jn.00604.2005 ◽

2005 ◽

Vol 94 (6) ◽

pp. 4196-4208 ◽

Cited By ~ 24

Author(s):

Ajithkumar Warrier ◽

Salvador Borges ◽

David Dalcino ◽

Cameron Walters ◽

Martin Wilson

Keyword(s):

Transmitter Release ◽

Metabotropic Glutamate Receptor ◽

Amacrine Cell ◽

Ryanodine Receptors ◽

Amacrine Cells ◽

Gaba Release ◽

Voltage Gated ◽

Metabotropic Glutamate ◽

Inositol 1,4,5 Trisphosphate ◽

Evoked Transmitter Release

The Ca2+ that promotes transmitter release is generally thought to enter presynaptic terminals through voltage-gated Ca2+channels. Using electrophysiology and Ca2+ imaging, we show that, in amacrine cell dendrites, at least some of the Ca2+ that triggers transmitter release comes from endoplasmic reticulum Ca2+ stores. We show that both inositol 1,4,5-trisphosphate receptors (IP3Rs) and ryanodine receptors (RyRs) are present in these dendrites and both participate in the elevation of cytoplasmic [Ca2+] during the brief depolarization of a dendrite. Only the Ca2+ released through IP3Rs, however, seems to promote the release of transmitter. Antagonists for the IP3R reduced transmitter release, whereas RyR blockers had no effect. Application of an agonist for metabotropic glutamate receptor, known to liberate Ca2+ from internal stores, enhanced both spontaneous and evoked transmitter release.

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A high-density narrow-field inhibitory retinal interneuron with direct coupling to Müller glia

10.1101/2020.01.23.917096 ◽

2020 ◽

Author(s):

William N Grimes ◽

Didem Göz Aytürk ◽

Mrinalini Hoon ◽

Takeshi Yoshimatsu ◽

Clare Gamlin ◽

...

Keyword(s):

Gap Junctions ◽

Glial Cells ◽

Amacrine Cell ◽

Electrical Coupling ◽

Amacrine Cells ◽

Muller Glia ◽

Müller Glia ◽

Cell Type ◽

Mammalian Retina ◽

Ganglion Neurons

AbstractAmacrine cells are interneurons comprising the most diverse cell type in the mammalian retina. They help encode visual features such as edges or directed motion by mediating excitatory and inhibitory interactions between input (i.e. bipolar) and output (i.e. ganglion) neurons in the inner plexiform layer (IPL). Like other brain regions, the retina also contains glial cells that contribute to neurotransmitter uptake, neurovascular control and metabolic regulation. Here, we report that a previously poorly characterized, but relatively abundant, inhibitory amacrine cell type in the mouse retina is coupled directly to Müller glia. Electron microscopic reconstructions of this amacrine type revealed extensive associations with Müller glia, whose processes often completely ensheathe the neurites of this amacrine cell type. Microinjections of small tracer molecules into the somas of these amacrine cells led to selective labelling of nearby Müller glia, leading us to suggest the name “Müller glia-coupled amacrine cell” or MAC. Our electrophysiological data also indicate that MACs release glycine at conventional chemical synapses with amacrine, bipolar and retinal ganglion cells (RGCs), and viral transsynaptic tracing showed connections to several known RGC types. Visually-evoked responses revealed a strong preference for light increments; these “ON” responses were primarily mediated by excitatory chemical synaptic input and direct electrical coupling to other cells. This initial characterization of the MAC provides the first evidence for neuron-glia coupling in the mammalian retina and identifies the MAC as a potential link between inhibitory processing and glial function.Significance StatementGap junctions between pairs of neurons or glial cells are commonly found throughout the nervous system, and play a myriad of roles including electrical coupling and metabolic exchange. In contrast, gap junctions between neurons and glia cells are rare and poorly understood. Here we report the first evidence for neuron-glia coupling in the mammalian retina, specifically between an abundant (but previously unstudied) inhibitory interneuron and Müller glia.

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Dopamine D1 receptor activation contributes to light-adapted changes in retinal inhibition to rod bipolar cells

Journal of Neurophysiology ◽

10.1152/jn.00855.2017 ◽

2018 ◽

Vol 120 (2) ◽

pp. 867-879 ◽

Cited By ~ 6

Author(s):

Michael D. Flood ◽

Johnnie M. Moore-Dotson ◽

Erika D. Eggers

Keyword(s):

Light Adaptation ◽

Amacrine Cell ◽

Amacrine Cells ◽

Receptor Activation ◽

Bipolar Cells ◽

D1 Receptor ◽

D1 Receptors ◽

Light Responses ◽

Dopamine Modulation ◽

Rod Bipolar Cells

Dopamine modulation of retinal signaling has been shown to be an important part of retinal adaptation to increased background light levels, but the role of dopamine modulation of retinal inhibition is not clear. We previously showed that light adaptation causes a large reduction in inhibition to rod bipolar cells, potentially to match the decrease in excitation after rod saturation. In this study, we determined how dopamine D1 receptors in the inner retina contribute to this modulation. We found that D1 receptor activation significantly decreased the magnitude of inhibitory light responses from rod bipolar cells, whereas D1 receptor blockade during light adaptation partially prevented this decline. To determine what mechanisms were involved in the modulation of inhibitory light responses, we measured the effect of D1 receptor activation on spontaneous currents and currents evoked from electrically stimulating amacrine cell inputs to rod bipolar cells. D1 receptor activation decreased the frequency of spontaneous inhibition with no change in event amplitudes, suggesting a presynaptic change in amacrine cell activity in agreement with previous reports that rod bipolar cells lack D1 receptors. Additionally, we found that D1 receptor activation reduced the amplitude of electrically evoked responses, showing that D1 receptors can modulate amacrine cells directly. Our results suggest that D1 receptor activation can replicate a large portion but not all of the effects of light adaptation, likely by modulating release from amacrine cells onto rod bipolar cells. NEW & NOTEWORTHY We demonstrated a new aspect of dopaminergic signaling that is involved in mediating light adaptation of retinal inhibition. This D1 receptor-dependent mechanism likely acts through receptors located directly on amacrine cells, in addition to its potential role in modulating the strength of serial inhibition between amacrine cells. Our results also suggest that another D2/D4 receptor-dependent or dopamine-independent mechanism must also be involved in light adaptation of inhibition to rod bipolar cells.

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

Visual Neuroscience ◽

10.1017/s0952523811000137 ◽

2011 ◽

Vol 28 (3) ◽

pp. 193-204 ◽

Cited By ~ 11

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.

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Multiple subtypes of glycine-immunoreactive neurons in the goldfish retina: Single- and double-label studies

Visual Neuroscience ◽

10.1017/s0952523800003424 ◽

1990 ◽

Vol 4 (3) ◽

pp. 299-309 ◽

Cited By ~ 17

Author(s):

Stephen Yazulla ◽

Keith M. Studholme

Keyword(s):

Substance P ◽

Visual Information ◽

Plexiform Layer ◽

Amacrine Cells ◽

Inner Plexiform Layer ◽

Double Labeling ◽

Light Microscopical Level ◽

Double Label ◽

Dendritic Stratification ◽

Goldfish Retina

AbstractThe glycinergic system in goldfish retina was studied by immunocytochemical localization of glycine antiserum at the light-microscopical level. Numerous amacrine cells, a type of interplexiform cell, interstitial cell, and displaced amacrine cell were glycine-immunoreactive (IR). Amacrine cells, accounting for 97% of the glycine-IR neurons, were of four types based solely on their level of dendritic stratification: stratified amacrine cells of the first, third, and fifth sublayers and bistratified amacrine cells of the first and fifth sublayers. Double-labeling experiments were carried out to determine possible co-localization of glycine-IR with GABA-IR, serotonin-IR, substance P-IR and somatostatin-IR. No evidence for co-localization of glycine-IR with these other transmitter substances was found, despite reports of co-localization of these substances in retinas of other species. Glycinergic neurons in goldfish retina appear to consist of a heterogeneous population of at least seven morphologically distinct subtypes that are also neurochemically distinct in regard to GABA, serotonin, substance P, and somatostatin. Since dendritic stratification in the inner plexiform layer is correlated with ON-, OFF-response types, we suggest that the subtypes of glycine-IR amacrine cells play different roles in the encoding of visual information.

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Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina

Development ◽

10.1242/dev.126.3.555 ◽

1999 ◽

Vol 126 (3) ◽

pp. 555-566 ◽

Cited By ~ 6

Author(s):

M.J. Belliveau ◽

C.L. Cepko

Keyword(s):

Progenitor Cells ◽

Cell Fate ◽

Progenitor Cell ◽

Amacrine Cell ◽

Amacrine Cells ◽

Environment Change ◽

Rat Retina ◽

Cell Fate Decisions ◽

Cone Cells ◽

Postnatal Environment

The seven major classes of cells of the vertebrate neural retina are generated from a pool of multipotent progenitor cells. Recent studies suggest a model of retinal development in which both the progenitor cells and the environment change over time (Cepko, C. L., Austin, C. P., Yang, X., Alexiades, M. and Ezzeddine, D. (1996). Proc. Natl. Acad. Sci. USA 93, 589–595). We have utilized a reaggregate culture system to test this model. A labeled population of progenitors from the embryonic rat retina were cultured with an excess of postnatal retinal cells and then assayed for their cell fate choices. We found that the postnatal environment had at least two signals that affected the embryonic cells' choice of fate; one signal inhibited the production of amacrine cells and a second affected the production of cone cells. No increase in cell types generated postnatally was observed. The source of the inhibitor of the amacrine cell fate appeared to be previously generated amacrine cells, suggesting that amacrine cell number is controlled by feedback inhibition. The progenitor cell lost its ability to be inhibited for production of an amacrine cell as it entered M phase of the cell cycle. We suggest that postmitotic cells influence progenitor cell fate decisions, but that they do so in a manner restricted by the intrinsic biases of progenitor cells.

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Dissection of the neuron network in the catfish inner retina. V. Interactions between NA and NB amacrine cells

Journal of Neurophysiology ◽

10.1152/jn.1990.63.1.120 ◽

1990 ◽

Vol 63 (1) ◽

pp. 120-130 ◽

Cited By ~ 20

Author(s):

H. M. Sakai ◽

K. I. Naka

Keyword(s):

White Noise ◽

Small Amplitude ◽

Amacrine Cell ◽

Amacrine Cells ◽

The Other ◽

First Order ◽

Membrane Noise ◽

Current Pulses ◽

Damped Oscillation ◽

Order Kernel

1. Simultaneous intracellular recordings were made from two neighboring N amacrine cells, one an ON amacrine (NA) cell and the other an OFF amacrine (NB) cell. Extrinsic current was injected into one amacrine cell, and the resulting intracellular responses were recorded from the other amacrine cell. Test signals included 1) a single-frequency sinusoid, 2) a depolarizing or hyperpolarizing pulse, or 3) a white-noise modulated current. In some cell pairs, membrane noise was measured in the dark as well as under a steady background illumination. 2. Current pulses injected into a NA cell evoked a damped oscillation from a NB cell. The first-order kernel derived by cross-correlating the white-noise current injected into a NA cell against the evoked response from a NB cell was a large depolarization followed by a damped oscillation. The frequency of oscillations varied slightly from pair to pair but averaged 35 Hz. 3. Current pulses injected into a NB cell evoked a sign-inverting response (hyperpolarization) of very small amplitude from a NA cell. Similarly, the first-order kernel was a hyperpolarization of very small amplitude. 4. The power spectrum of the membrane noise recorded from NA and NB cells in the dark or during steady illumination often showed a peak at 35 Hz. Such membrane noise synchronizes synergistically among NA cells and among NB cells in the dark. In addition, the membrane fluctuations seen in NA and NB cells in the dark were out of phase. 5. Transmission between NA and NB cells was largely accounted for by a linear component; however, a very small but significant second- and third-order nonlinearity was also generated. 6. These results show that the interactions occurring between amacrine cells of opposite response polarity are much more complex than those between cells of the same response polarity and that the neural circuitry in the inner retina actively controls interactions between ON and OFF channels in the dark as well as in the presence of light stimuli.

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