Membrane properties of an unusual intrinsically oscillating, wide‐field teleost retinal amacrine cell

At early stages of visual processing, receptive fields are typically described as subtending local regions of space and thus performing computations on a narrow spatial scale. Nevertheless, stimulation well outside of the classical receptive field can exert clear and significant effects on visual processing. Given the distances over which they occur, the retinal mechanisms responsible for these long-range effects would certainly require signal propagation via active membrane properties. Here the physiology of a wide-field amacrine cell—the wiry cell—in macaque monkey retina is explored, revealing receptive fields that represent a striking departure from the classic structure. A single wiry cell integrates signals over wide regions of retina, 5–10 times larger than the classic receptive fields of most retinal ganglion cells. Wiry cells integrate signals over space much more effectively than predicted from passive signal propagation, and spatial integration is strongly attenuated during blockade of NMDA spikes but integration is insensitive to blockade of NaV channels with TTX. Thus these cells appear well suited for contributing to the long-range interactions of visual signals that characterize many aspects of visual perception.

Download Full-text

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.

Download Full-text

Wide‐field amacrine cell inputs to ON parasol ganglion cells in macaque retina

The Journal of Comparative Neurology ◽

10.1002/cne.24840 ◽

2019 ◽

Vol 528 (9) ◽

pp. 1588-1598 ◽

Cited By ~ 1

Author(s):

Sara S. Patterson ◽

Andrea S. Bordt ◽

Rebecca J. Girresch ◽

Conor M. Linehan ◽

Jacob Bauss ◽

...

Keyword(s):

Amacrine Cell ◽

Ganglion Cells ◽

Wide Field

Download Full-text

Direction selectivity in a model of the starburst amacrine cell

Visual Neuroscience ◽

10.1017/s0952523804214109 ◽

2004 ◽

Vol 21 (4) ◽

pp. 611-625 ◽

Cited By ~ 54

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.

Download Full-text

Morphological and physiological properties of the A17 amacrine cell of the rat retina

Visual Neuroscience ◽

10.1017/s0952523800175108 ◽

2000 ◽

Vol 17 (5) ◽

pp. 769-780 ◽

Cited By ~ 43

Author(s):

NICOLE MENGER ◽

HEINZ WÄSSLE

Keyword(s):

Amacrine Cell ◽

Light Stimulus ◽

Plexiform Layer ◽

Light Response ◽

Amacrine Cells ◽

Wide Field ◽

Inner Plexiform Layer ◽

Cell Type ◽

Full Field ◽

Rat Retina

In addition to the well-studied AII amacrine cell, there is another amacrine cell type participating in the rod pathway of the mammalian retina. In cat, this cell is called the A17 amacrine cell, and in rabbits, it is called the indoleamine-accumulating amacrine cell (S1 and S2); however, the presence of the corresponding cell type has not yet been described in detail for the rat retina. To this end, we injected amacrine cells with Neurobiotin in vertical retinal slices. After histological processing, we were able to reconstruct the morphology of a wide-field amacrine cell which showed characteristics of A17 and S1/S2 amacrine cells. The rat wide-field amacrine cells exhibited the same stratification pattern, their dendrites bore varicosities and ramified in sublamina 5 of the inner plexiform layer (IPL), and they were dye-coupled to other amacrine cells. To determine whether those amacrine cells shared electrophysiological characteristics as well, we performed whole-cell patch-clamp recordings and examined their voltage-activated currents and neurotransmitter-induced currents. We never observed voltage-gated Na+ currents and spike-like potentials upon depolarization by current injection in these cells. We identified GABA- and glycine-sensitive Cl− currents that could be blocked by bicuculline and strychnine, respectively. We also observed kainate- and AMPA-activated currents, which could be inhibited by the application of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX). Finally, a 400-ms full-field light stimulus was used to characterize the light responses of A17 amacrine cells. The light ON-induced inward current could be suppressed by the application of 2,3-Dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulphonamide (NBQX), while the majority of the light OFF-induced current was inhibited by bicuculline and reduced to a smaller extent by NBQX. CPP, an NMDA blocker, had no effect on the light response of rat A17 amacrine cells.

Download Full-text

Receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells

Visual Neuroscience ◽

10.1017/s0952523800007409 ◽

1995 ◽

Vol 12 (1) ◽

pp. 177-184 ◽

Cited By ~ 15

Author(s):

Ralph J. Jensen

Keyword(s):

Receptive Field ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Membrane Properties ◽

Optic Disk ◽

Receptive Field Properties ◽

Tungsten Microelectrode ◽

Starburst Amacrine Cells ◽

Starburst Amacrine Cell

AbstractStarburst amacrine cells in the rabbit retina were labeled following an intraocular injection of the fluorescent dye, 4, 6, diamidino-2-phenylindole (DAPI). From each eye a strip of retina was removed, mounted on a platform beneath an epifluorescence microscope, and superfused with a physiological solution. The tip of a tungsten microelectrode (for extracellular recording) was visually positioned near the cell body of a DAPI-labeled starburst amacrine cell that was located in the ganglion cell layer. Light-evoked responses from the displaced starburst amacrine cells were studied in normal retinas and in retinas that had received a small electrolytic lesion near the optic disk 5–9 months beforehand. In normal retinas, a small spot of light centered over the receptive field of a displaced starburst amacrine cell in nearly all cases evoked a brief burst of spikes only at light onset. When stimulated with a large spot or an annulus of light, many cells gave a small burst of spikes at light offset. In lesioned retinas, the light responses of displaced starburst amacrine cells were recorded in areas of the retina where ganglion cells had degenerated. All cells responded with a large burst of spikes at the onset and offset of a small, centered spot of light. Large spots and annuli of light also evoked robust ON/OFF responses from these cells. The results from this study show that the receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells. This finding indicates that changes in either synaptic transmission or the membrane properties of neurons occur in the retina following degeneration of ganglion cells.

Download Full-text

Ionotropic glutamate receptors of amacrine cells of the mouse retina

Visual Neuroscience ◽

10.1017/s0952523806231079 ◽

2006 ◽

Vol 23 (1) ◽

pp. 79-90 ◽

Cited By ~ 15

Author(s):

OLIVIA N. DUMITRESCU ◽

DARIO A. PROTTI ◽

SRIPARNA MAJUMDAR ◽

HANNS ULRICH ZEILHOFER ◽

HEINZ WÄSSLE

Keyword(s):

Nmda Receptors ◽

Glutamate Receptors ◽

Amacrine Cell ◽

Fluorescent Protein ◽

Lucifer Yellow ◽

Amacrine Cells ◽

Ionotropic Glutamate Receptors ◽

Mouse Retina ◽

Wide Field ◽

Transgenic Mouse Line

The mammalian retina contains approximately 30 different morphological types of amacrine cells, receiving glutamatergic input from bipolar cells. In this study, we combined electrophysiological and pharmacological techniques in order to study the glutamate receptors expressed by different types of amacrine cells. Whole-cell currents were recorded from amacrine cells in vertical slices of the mouse retina. During the recordings the cells were filled with Lucifer Yellow/Neurobiotin allowing classification as wide-field or narrow-field amacrine cells. Amacrine cell recordings were also carried out in a transgenic mouse line whose glycinergic amacrine cells express enhanced green fluorescent protein (EGFP). Agonist-induced currents were elicited by exogenous application of NMDA, AMPA, and kainate (KA) while holding cells at −75 mV. Using a variety of specific agonists and antagonists (NBQX, AP5, cyclothiazide, GYKI 52466, GYKI 53655, SYM 2081) responses mediated by AMPA, KA, and NMDA receptors could be dissected. All cells (n= 300) showed prominent responses to non-NMDA agonists. Some cells expressed AMPA receptors exclusively and some cells expressed KA receptors exclusively. In the majority of cells both receptor types could be identified. NMDA receptors were observed in about 75% of the wide-field amacrine cells and in less than half of the narrow-field amacrine cells. Our results confirm that different amacrine cell types express distinct sets of ionotropic glutamate receptors, which may be critical in conferring their unique temporal responses to this diverse neuronal class.

Download Full-text

Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1980.0060 ◽

1980 ◽

Vol 208 (1173) ◽

pp. 415-431 ◽

Cited By ~ 97

Keyword(s):

Ganglion Cell ◽

Amacrine Cell ◽

Ganglion Cell Layer ◽

Cell Layer ◽

Amacrine Cells ◽

Cell System ◽

Wide Field ◽

Dendritic Field ◽

Displaced Amacrine Cells ◽

Bistratified Cell

The amacrine cells in the retina of the rat are described in Golgi-stained whole-mounted retinae. Nine morphologically distinct types of cell were found: one type of diffuse cell, five types of unistratified cell, two types of bistratified cell, and one type of stratified diffuse cell. Measurements show that the largest unistratified cells have a dendritic field 2 mm across. One type of interplexiform cell is also described. Wide-field diffuse amacrine cells and unistratified amacrine cells were found with their somata located in either the inner nuclear layer or the ganglion cell layer. It is clear that there may be an amacrine cell system in the ganglion cell layer of the rat retina.

Download Full-text

Response properties of a unique subtype of wide-field amacrine cell in the rabbit retina

Visual Neuroscience ◽

10.1017/s0952523807070071 ◽

2007 ◽

Vol 24 (4) ◽

pp. 459-469 ◽

Cited By ~ 21

Author(s):

STEWART A. BLOOMFIELD ◽

BÉLA VÖLGYI

Keyword(s):

Receptive Field ◽

Amacrine Cell ◽

Receptive Fields ◽

Amacrine Cells ◽

Dendritic Morphology ◽

Dendritic Arbor ◽

Wide Field ◽

Rabbit Retina ◽

Spatial Disparity ◽

Voltage Gated Sodium Channels

We studied the morphology and physiology of a unique wide-field amacrine cell in the rabbit retina. These cells displayed a stereotypic dendritic morphology consisting of a large, circular and monostratified arbor that often extended over 2 mm. Their responses contained both somatic and dendritic sodium spikes suggesting active propagation of synaptic signals within the dendritic arbor. This idea is supported by the enormous size of their ON-OFF receptive fields. Interestingly, these cells exhibited separate ON and OFF receptive fields that, while concentric, were vastly different in size. Whereas the ON receptive field of these cells extended nearly 2 mm, the OFF receptive field was typically 75% smaller. Blockade of voltage-gated sodium channels with QX-314 dramatically reduced the large ON receptive field, but had little effect on the smaller OFF receptive field. These results indicate a spatial disparity in the location of on- and off-center bipolar cell inputs to the dendritic arbor of wide-field amacrine cells. In addition, the active propagation of signals suggests that synaptic inputs are integrated both locally and globally within the dendritic arbor.

Download Full-text

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

The Journal of General Physiology ◽

10.1085/jgp.84.6.915 ◽

1984 ◽

Vol 84 (6) ◽

pp. 915-925 ◽

Cited By ~ 38

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.

Download Full-text