Electrical Coupling and Passive Membrane Properties of AII Amacrine Cells

2010 ◽  
Vol 103 (3) ◽  
pp. 1456-1466 ◽  
Author(s):  
Margaret Lin Veruki ◽  
Leif Oltedal ◽  
Espen Hartveit
Keyword(s):  
Amacrine Cell ◽  
Electrical Coupling ◽  
Amacrine Cells ◽  
Input Resistance ◽  
Membrane Resistance ◽  
Membrane Properties ◽  
Total Input ◽  
Junctional Conductance ◽  
Aii Amacrine Cells ◽  
Aii Amacrine

AII amacrine cells in the mammalian retina are connected via electrical synapses to on-cone bipolar cells and to other AII amacrine cells. To understand synaptic integration in these interneurons, we need information about the junctional conductance ( gj), the membrane resistance ( rm), the membrane capacitance ( Cm), and the cytoplasmic resistivity ( Ri). Due to the extensive electrical coupling, it is difficult to obtain estimates of rm, as well as the relative contribution of the junctional and nonjunctional conductances to the total input resistance of an AII amacrine cell. Here we used dual voltage-clamp recording of pairs of electrically coupled AII amacrine cells in an in vitro slice preparation from rat retina and applied meclofenamic acid (MFA) to block the electrical coupling and isolate single AII amacrines electrically. In the control condition, the input resistance ( Rin) was ∼620 MΩ and the apparent rm was ∼760 MΩ. After block of electrical coupling, determined by estimating gj in the dual recordings, Rin and rm were ∼4,400 MΩ, suggesting that the nongap junctional conductance of an AII amacrine cell is ∼16% of the total input conductance. Control experiments with nucleated patches from AII amacrine cells suggested that MFA had no effect on the nongap junctional membrane of these cells. From morphological reconstructions of AII amacrine cells filled with biocytin, we obtained a surface area of ∼900 μm2 which, with a standard value for Cm of 0.01 pF/μm2, corresponds to an average capacitance of ∼9 pF and a specific membrane resistance of ∼41 kΩ cm2. Together with information concerning synaptic connectivity, these data will be important for developing realistic compartmental models of the network of AII amacrine cells.

Electrical Synapses Between AII Amacrine Cells: Dynamic Range and Functional Consequences of Variation in Junctional Conductance

2008 ◽  
Vol 100 (6) ◽  
pp. 3305-3322 ◽  
Author(s):  
Margaret Lin Veruki ◽  
Leif Oltedal ◽  
Espen Hartveit
Keyword(s):  
Dynamic Range ◽  
Amacrine Cells ◽  
Electrical Synapses ◽  
Pass Filter ◽  
Low Pass Filter ◽  
Junctional Conductance ◽  
Coupled Cells ◽  
Functional Consequences ◽  
Aii Amacrine Cells ◽  
Aii Amacrine

AII amacrine cells form a network of electrically coupled interneurons in the mammalian retina and tracer coupling studies suggest that the junctional conductance ( Gj) can be modulated. However, the dynamic range of Gj and the functional consequences of varying Gj over the dynamic range are unknown. Here we use whole cell recordings from pairs of coupled AII amacrine cells in rat retinal slices to provide direct evidence for physiological modulation of Gj, appearing as a time-dependent increase from about 500 pS to a maximum of about 3,000 pS after 30–90 min of recording. The increase occurred in recordings with low- but not high-resistance pipettes, suggesting that it was related to intracellular washout and perturbation of a modulatory system. Computer simulations of a network of electrically coupled cells verified that our recordings were able to detect and quantify changes in Gj over a large range. Dynamic-clamp electrophysiology, with insertion of electrical synapses between AII amacrine cells, allowed us to finely and reversibly control Gj within the same range observed for physiologically coupled cells and to examine the quantitative relationship between Gj and steady-state coupling coefficient, synchronization of subthreshold membrane potential fluctuations, synchronization and transmission of action potentials, and low-pass filter characteristics. The range of Gj values over which signal transmission was modulated depended strongly on the specific functional parameter examined, with the largest range observed for action potential transmission and synchronization, suggesting that the full range of Gj values observed during spontaneous run-up of coupling could represent a physiologically relevant dynamic range.

Light-induced modulation of coupling between AII amacrine cells in the rabbit retina

1997 ◽  
Vol 14 (3) ◽  
pp. 565-576 ◽  
Author(s):  
Stewart A. Bloomfield ◽  
Daiyan Xin ◽  
Tristan Osborne
Keyword(s):  
Receptive Field ◽  
Gap Junctions ◽  
Electrical Coupling ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Field Size ◽  
Background Illumination ◽  
Aii Amacrine Cells ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

AbstractThe rod-driven, AII amacrine cells in the mammalian retina maintain homologous gap junctions with one another as well as heterologous gap junctions with on-cone bipolar cells. We used background illumination to study whether changes in the adaptational state of the retina affected the permeabilities of these two sets of gap junctions. To access changes in permeability, we injected single AII amacrine cells with the biotinylated tracer, Neurobiotin, and measured the extent of tracer coupling to neighboring AII cells and neighboring cone bipolar cells. We also measured the center-receptive field size of All cells to assess concomitant changes in electrical coupling. Our results indicate that in well dark-adapted retinas, AII cells form relatively small networks averaging 20 amacrine cells and covering about 75 μm. The size of these networks matched closely to the size of AII cell on-center receptive fields. However, over most of their operating range, AII cells formed dramatically larger networks, averaging 326 amacrine cells, which corresponded to an increased receptive-field size. As the retina was light adapted beyond the operating range of the AII cells, they uncoupled to form networks comparable in size to those seen in well dark-adapted retinas. Our results, then, indicate that the adaptational state of the retina has a profound effect on the extent of electrical coupling between AII amacrine cells. Although we observed light-induced changes in the number of tracer-coupled cone bipolar cells, these appeared to be an epiphenomenon of changes in homologous coupling between AII amacrine cells. Therefore, in contrast to the robust changes in AII–AII coupling produced by background illumination, our data provided no evidence of a light-induced modulation of coupling between AII cells and on-cone bipolar cells.

scholarly journals Application of transretinal current stimulation for the study of bipolar-amacrine transmission.

1984 ◽  
Vol 84 (6) ◽  
pp. 915-925 ◽  
Author(s):  
J Toyoda ◽  
M Fujimoto
Keyword(s):  
Amacrine Cell ◽  
Light Response ◽  
Amacrine Cells ◽  
Membrane Resistance ◽  
Ringer Solution ◽  
Bipolar Cells ◽  
Membrane Properties ◽  
Axon Terminals ◽  
Transient Nature ◽  
Hyperpolarizing Response

Transretinal current flowing from the receptor side to the vitreous side depolarizes the axon terminals of retinal cells and facilitates the release of transmitter. Such current elicited a depolarizing response in off-center bipolar cells and a hyperpolarizing response in on-center bipolar cells. It also elicited a response of relatively complex waveform in amacrine cells. The responses elicited in bipolar cells were suppressed in the presence of 5-10 mM glutamate in the perfusing Ringer solution, while the responses of amacrine cells persisted, although their waveform changed to a simple one that showed monotonic depolarization irrespective of the type of amacrine cell and were accompanied by a decrease in the membrane resistance. The results indicate excitatory synaptic transmission from bipolar cells to amacrine cells. Since the response elicited by current in ON-OFF cells was almost identical to those elicited in ON or OFF amacrine cells, the transient nature of their light response cannot be due to their membrane properties. ON-OFF cells responded to transretinal current flowing in the opposite direction with a small hyperpolarization accompanied by a resistance increase. The hyperpolarizing response was suppressed by the addition of GABA in glutamate Ringer solution. The results suggest an activation by the current of GABA-ergic feedback pathways from amacrine cells to bipolar cells.

scholarly journals The somal patterning of the AII amacrine cell mosaic in the mouse retina is indistinguishable from random simulations matched for density and constrained by soma size

2018 ◽  
Vol 35 ◽  
Author(s):  
PATRICK W. KEELEY ◽  
BENJAMIN E. REESE
Keyword(s):  
Amacrine Cell ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Mouse Retina ◽  
Retinal Neurons ◽  
Soma Size ◽  
Aii Amacrine Cells ◽  
Aii Amacrine ◽  
Cholinergic Amacrine Cells

AbstractThe orderly spacing of retinal neurons is commonly regarded as a characteristic feature of retinal nerve cell populations. Exemplars of this property include the horizontal cells and the cholinergic amacrine cells, where individual cells minimize the proximity to like-type neighbors, yielding regularity in the patterning of their somata. Recently, two types of retinal bipolar cells in the mouse retina were shown to exhibit an order in their somal patterning no different from density-matched simulations constrained by soma size but being otherwise randomly distributed. The present study has now extended this finding to a type of retinal amacrine cell, the AII amacrine cell. Voronoi domain analysis revealed the patterning in the population of AII amacrine somata to be no different from density-matched and soma-size-constrained random simulations, while analysis of the density recovery profile showed AII amacrine cells to exhibit a minimal intercellular spacing identical to that for those random simulations: AII amacrine somata were positioned side-by-side as often as chance would predict. Regularity indexes and packing factors (PF) were far lower than those achieved by either the horizontal cells or cholinergic amacrine cells, with PFs also being comparable to those derived from the constrained random simulations. These results extend recent findings that call into question the widespread assumption that all types of retinal neurons are assembled as regular somal arrays, and have implications for the way in which AII amacrine cells must distribute their processes to ensure a uniform coverage of the retinal surface.

scholarly journals Intrinsic bursting of AII amacrine cells underlies oscillations in the rd1 mouse retina

2014 ◽  
Vol 112 (6) ◽  
pp. 1491-1504 ◽  
Author(s):  
Hannah Choi ◽  
Lei Zhang ◽  
Mark S. Cembrowski ◽  
Carl F. Sabottke ◽  
Alexander L. Markowitz ◽  
...  
Keyword(s):  
Amacrine Cell ◽  
Ganglion Cells ◽  
Wild Type Mouse ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Membrane Properties ◽  
Mouse Retina ◽  
Intrinsic Membrane Properties ◽  
Rd1 Mouse ◽  
Aii Amacrine

In many forms of retinal degeneration, photoreceptors die but inner retinal circuits remain intact. In the rd1 mouse, an established model for blinding retinal diseases, spontaneous activity in the coupled network of AII amacrine and ON cone bipolar cells leads to rhythmic bursting of ganglion cells. Since such activity could impair retinal and/or cortical responses to restored photoreceptor function, understanding its nature is important for developing treatments of retinal pathologies. Here we analyzed a compartmental model of the wild-type mouse AII amacrine cell to predict that the cell's intrinsic membrane properties, specifically, interacting fast Na and slow, M-type K conductances, would allow its membrane potential to oscillate when light-evoked excitatory synaptic inputs were withdrawn following photoreceptor degeneration. We tested and confirmed this hypothesis experimentally by recording from AIIs in a slice preparation of rd1 retina. Additionally, recordings from ganglion cells in a whole mount preparation of rd1 retina demonstrated that activity in AIIs was propagated unchanged to elicit bursts of action potentials in ganglion cells. We conclude that oscillations are not an emergent property of a degenerated retinal network. Rather, they arise largely from the intrinsic properties of a single retinal interneuron, the AII amacrine cell.

scholarly journals AII amacrine cells discriminate between heterocellular and homocellular locations when assembling connexin36-containing gap junctions

2014 ◽  
Vol 127 (6) ◽  
pp. 1190-1202 ◽  
Author(s):  
A. Meyer ◽  
G. Hilgen ◽  
B. Dorgau ◽  
E. M. Sammler ◽  
R. Weiler ◽  
...  
Keyword(s):  
Gap Junctions ◽  
Amacrine Cells ◽  
Aii Amacrine Cells ◽  
Aii Amacrine

Meclofenamic Acid Blocks Electrical Synapses of Retinal AII Amacrine and on-Cone Bipolar Cells

2009 ◽  
Vol 101 (5) ◽  
pp. 2339-2347 ◽  
Author(s):  
Margaret Lin Veruki ◽  
Espen Hartveit
Keyword(s):  
Amacrine Cells ◽  
Bipolar Cells ◽  
Electrical Synapse ◽  
Dependent Manner ◽  
Electrical Synapses ◽  
Meclofenamic Acid ◽  
Aii Amacrine Cells ◽  
Rod Pathway ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

Gap junction channels constitute specialized intercellular contacts that can serve as electrical synapses. In the rod pathway of the retina, electrical synapses between AII amacrine cells express connexin 36 (Cx36) and electrical synapses between AII amacrines and on-cone bipolar cells express Cx36 on the amacrine side and Cx36 or Cx45 on the bipolar side. For physiological investigations of the properties and functions of these electrical synapses, it is highly desirable to have access to potent pharmacological blockers with selective and reversible action. Here we use dual whole cell voltage-clamp recordings of pairs of AII amacrine cells and pairs of AII amacrine and on-cone bipolar cells in rat retinal slices to directly measure the junctional conductance ( Gj) between electrically coupled cells and to study the effect of the drug meclofenamic acid (MFA) on Gj. Consistent with previous tracer coupling studies, we found that MFA reversibly blocked the electrical synapse currents in a concentration-dependent manner, with complete block at 100 μM. Whereas MFA evoked a detectable decrease in Gj within minutes of application, the time to complete block of Gj was considerably longer, typically 20–40 min. After washout, Gj recovered to 20–90% of the control level, but the time to maximum recovery was typically >1 h. These results suggest that MFA can be a useful drug to investigate the physiological functions of electrical synapses in the rod pathway, but that the slow kinetics of block and reversal might compromise interpretation of the results and that explicit monitoring of Gj is desirable.

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

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.

scholarly journals Spikelets and bursts in axonless retinal AII amacrine cells coupled by gap junctions

2013 ◽  
Vol 14 (S1) ◽  
Author(s):  
Hermann Riecke ◽  
Hannah Choi ◽  
Mark S Cembrowski ◽  
William L Kath ◽  
Joshua H Singer
Keyword(s):  
Gap Junctions ◽  
Amacrine Cells ◽  
Aii Amacrine Cells ◽  
Aii Amacrine
Sign in / Sign up

Export Citation Format

Share Document