Dendritic and parallel processing of visual threats in the retina control defensive responses

Approaching predators cast expanding shadows (i.e., looming) that elicit innate defensive responses in most animals. Where looming is first detected and how critical parameters of predatory approaches are extracted are unclear. In mice, we identify a retinal interneuron (the VG3 amacrine cell) that responds robustly to looming, but not to related forms of motion. Looming-sensitive calcium transients are restricted to a specific layer of the VG3 dendrite arbor, which provides glutamatergic input to two ganglion cells (W3 and OFFα). These projection neurons combine shared excitation with dissimilar inhibition to signal approach onset and speed, respectively. Removal of VG3 amacrine cells reduces the excitation of W3 and OFFα ganglion cells and diminishes defensive responses of mice to looming without affecting other visual behaviors. Thus, the dendrites of a retinal interneuron detect visual threats, divergent circuits downstream extract critical threat parameters, and these retinal computations initiate an innate survival behavior.

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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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Interneuron Circuits Tune Inhibition in Retinal Bipolar Cells

Journal of Neurophysiology ◽

10.1152/jn.00458.2009 ◽

2010 ◽

Vol 103 (1) ◽

pp. 25-37 ◽

Cited By ~ 45

Author(s):

Erika D. Eggers ◽

Peter D. Lukasiewicz

Keyword(s):

Ganglion Cell ◽

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Feedback Inhibition ◽

Amacrine Cells ◽

Bipolar Cells ◽

Light Stimuli ◽

Cell Inhibition ◽

Cell Networks

While connections between inhibitory interneurons are common circuit elements, it has been difficult to define their signal processing roles because of the inability to activate these circuits using natural stimuli. We overcame this limitation by studying connections between inhibitory amacrine cells in the retina. These interneurons form spatially extensive inhibitory networks that shape signaling between bipolar cell relay neurons to ganglion cell output neurons. We investigated how amacrine cell networks modulate these retinal signals by selectively activating the networks with spatially defined light stimuli. The roles of amacrine cell networks were assessed by recording their inhibitory synaptic outputs in bipolar cells that suppress bipolar cell output to ganglion cells. When the amacrine cell network was activated by large light stimuli, the inhibitory connections between amacrine cells unexpectedly depressed bipolar cell inhibition. Bipolar cell inhibition elicited by smaller light stimuli or electrically activated feedback inhibition was not suppressed because these stimuli did not activate the connections between amacrine cells. Thus the activation of amacrine cell circuits with large light stimuli can shape the spatial sensitivity of the retina by limiting the spatial extent of bipolar cell inhibition. Because inner retinal inhibition contributes to ganglion cell surround inhibition, in part, by controlling input from bipolar cells, these connections may refine the spatial properties of the retinal output. This functional role of interneuron connections may be repeated throughout the CNS.

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Heterocellular coupling between amacrine cell and ganglion cells

10.1101/328815 ◽

2018 ◽

Author(s):

Robert E. Marc ◽

Crystal Sigulinsky ◽

Rebecca L. Pfeiffer ◽

Daniel Emrich ◽

James R. Anderson ◽

...

Keyword(s):

Gap Junctions ◽

Ganglion Cell ◽

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Bipolar Cells ◽

Inner Plexiform Layer ◽

Tem Analysis

AbstractAll superclasses of retinal neurons display some form of electrical coupling including the key neurons of the inner plexiform layer: bipolar cells (BCs), amacrine or axonal cells (ACs) and ganglion cells (GCs). However, coupling varies extensively by class. For example, mammalian rod bipolar cells form no gap junctions at all, while all cone bipolar cells form class-specific coupling arrays, many of them homocellular in-superclass arrays. Ganglion cells are unique in that classes with coupling predominantly form heterocellular cross-class arrays of ganglion cell::amacrine cell (GC::AC) coupling in the mammalian retina. Ganglion cells are the least frequent superclass in the inner plexiform layer and GC::AC gap junctions are sparsely arrayed amidst massive cohorts of AC::AC, bipolar cell BC::BC, and AC::BC gap junctions. Many of these gap junctions and most ganglion cell gap junctions are suboptical, complicating analysis of specific ganglion cells. High resolution 2 nm TEM analysis of rabbit retinal connectome RC1 allows quantitative GC::AC coupling maps of identified ganglion cells. Ganglion cells classes apparently avoid direct cross-class homocellular coupling altogether even though they have opportunities via direct membrane touches, while transient OFF alpha ganglion cells and transient ON directionally selective (DS) ganglion cells are strongly coupled to distinct amacrine / axonal cell cohorts.A key feature of coupled ganglion cells is intercellular metabolite flux. Most GC::AC coupling involves GABAergic cells (γ+ amacrine cells), which results in significant GABA flux into ganglion cells. Surveying GABA coupling signatures in the ganglion cell layer across species suggests that the majority of vertebrate retinas engage in GC::AC coupling.Multi-hop synaptic queries of the entire RC1 connectome clearly profiles the coupled amacrine and axonal cells. Photic drive polarities and source bipolar cell class selec-tivities are tightly matched across coupled cells. OFF alpha ganglion cells are coupled to OFF γ+ amacrine cells and transient ON DS ganglion cells are coupled to ON γ+ amacrine cells including a large interstitial axonal cell (IAC). Synaptic tabulations show close matches between the classes of bipolar cells sampled by the coupled amacrine and ganglion cells. Further, both ON and OFF coupling ganglion networks show a common theme: synaptic asymmetry whereby the coupled γ+ neurons are also presynaptic to ganglion cell dendrites from different classes of ganglion cells outside the coupled set. In effect, these heterocellular coupling patterns enable an excited ganglion cell to directly inhibit nearby ganglion cells of different classes. Similarly, coupled γ+ amacrine cells engaged in feedback networks can leverage the additional gain of bipolar cell synapses in shaping the signaling of a spectrum of downstream targets based on their own selective coupling with ganglion cells.

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Disruption of transient photoreceptor targeting within the inner plexiform layer following early ablation of cholinergic amacrine cells in the ferret

Visual Neuroscience ◽

10.1017/s095252380118507x ◽

2001 ◽

Vol 18 (5) ◽

pp. 741-751 ◽

Cited By ~ 11

Author(s):

P.T. JOHNSON ◽

M.A. RAVEN ◽

B.E. REESE

Keyword(s):

Retinal Ganglion Cells ◽

Amacrine Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Subcutaneous Injections ◽

Cell Processes ◽

Cholinergic Amacrine Cells

Photoreceptors in the ferret's retina have been shown to project transiently to the inner plexiform layer (IPL) prior to their differentiation of an outer segment. On postnatal day 15 (P-15), when this projection achieves maximal density, the photoreceptors projecting into the IPL extend primarily to one of two depths, coincident with the processes of cholinergic amacrine cells. The present study has used an excitotoxic approach employing subcutaneous injections of l-glutamate to ablate these cholinergic amacrine cells on P-7, in order to see whether their elimination alters this targeting of photoreceptor terminals within the IPL. The near-complete elimination of cholinergic amacrine cells at P-15 was confirmed, although the population of retinal ganglion cells was also affected, being depleted by roughly 50%. The rod opsin-immunopositive terminals in such treated ferrets no longer showed a stratified distribution, being found throughout the depth of the IPL, as well as extending into the ganglion cell layer. This effect should not be due to the partial loss of retinal ganglion cells, however, since optic nerve transection at P-2, which eliminates the ganglion cells entirely while leaving the cholinergic amacrine cell population intact, was shown not to affect the stratification pattern of the photoreceptors within the IPL. These results strongly suggest that the targeting of the photoreceptor terminals to discrete strata within the IPL is dependent upon the cholinergic amacrine cell processes.

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Synaptic inputs from identified bipolar and amacrine cells to a sparsely branched ganglion cell in rabbit retina

Visual Neuroscience ◽

10.1017/s0952523819000014 ◽

2019 ◽

Vol 36 ◽

Cited By ~ 4

Author(s):

Andrea S. Bordt ◽

Diego Perez ◽

Luke Tseng ◽

Weiley Sunny Liu ◽

Jay Neitz ◽

...

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Bipolar Cells ◽

Rabbit Retina ◽

Retinal Ganglion ◽

Synaptic Inputs ◽

Class Iv

AbstractThere are more than 30 distinct types of mammalian retinal ganglion cells, each sensitive to different features of the visual environment. In rabbit retina, they can be grouped into four classes according to their morphology and stratification of their dendrites in the inner plexiform layer (IPL). The goal of this study was to describe the synaptic inputs to one type of Class IV ganglion cell, the third member of the sparsely branched Class IV cells (SB3). One cell of this type was partially reconstructed in a retinal connectome developed using automated transmission electron microscopy (ATEM). It had slender, relatively straight dendrites that ramify in the sublamina a of the IPL. The dendrites of the SB3 cell were always postsynaptic in the IPL, supporting its identity as a ganglion cell. It received 29% of its input from bipolar cells, a value in the middle of the range for rabbit retinal ganglion cells studied previously. The SB3 cell typically received only one synapse per bipolar cell from multiple types of presumed OFF bipolar cells; reciprocal synapses from amacrine cells at the dyad synapses were infrequent. In a few instances, the bipolar cells presynaptic to the SB3 ganglion cell also provided input to an amacrine cell presynaptic to the ganglion cell. There was apparently no crossover inhibition from narrow-field ON amacrine cells. Most of the amacrine cell inputs were from axons and dendrites of GABAergic amacrine cells, likely providing inhibitory input from outside the classical receptive field.

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Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

Visual Neuroscience ◽

10.1017/s0952523805224148 ◽

2005 ◽

Vol 22 (4) ◽

pp. 535-549 ◽

Cited By ~ 17

Author(s):

JIAN ZHANG ◽

WEI LI ◽

HIDEO HOSHI ◽

STEPHEN L. MILLS ◽

STEPHEN C. MASSEY

Keyword(s):

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Bipolar Cells ◽

Confocal Imaging ◽

Rabbit Retina ◽

Firing Rates ◽

Starburst Amacrine Cells ◽

Cholinergic Sensitivity

The correlation between cholinergic sensitivity and the level of stratification for ganglion cells was examined in the rabbit retina. As examples, we have used ON or OFF α ganglion cells and ON/OFF directionally selective (DS) ganglion cells. Nicotine, a cholinergic agonist, depolarized ON/OFF DS ganglion cells and greatly enhanced their firing rates but it had modest excitatory effects on ON or OFF α ganglion cells. As previously reported, we conclude that DS ganglion cells are the most sensitive to cholinergic drugs. Confocal imaging showed that ON/OFF DS ganglion cells ramify precisely at the level of the cholinergic amacrine cell dendrites, and co-fasciculate with the cholinergic matrix of starburst amacrine cells. However, neither ON or OFF α ganglion cells have more than a chance association with the cholinergic matrix. Z-axis reconstruction showed that OFF α ganglion cells stratify just below the cholinergic band in sublamina a while ON α ganglion cells stratify just below cholinergic b. The latter is at the same level as the terminals of calbindin bipolar cells. Thus, the calbindin bipolar cell appears to be a prime candidate to provide the bipolar cell input to ON α ganglion cells in the rabbit retina. We conclude that the precise level of stratification is correlated with the strength of cholinergic input. Alpha ganglion cells receive a weak cholinergic input and they are narrowly stratified just below the cholinergic bands.

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Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network

Visual Neuroscience ◽

10.1017/s0952523807070575 ◽

2007 ◽

Vol 24 (4) ◽

pp. 593-608 ◽

Cited By ~ 42

Author(s):

STEPHEN L. MILLS ◽

XIAO-BO XIA ◽

HIDEO HOSHI ◽

SALLY I. FIRTH ◽

MARGARET E. RICE ◽

...

Keyword(s):

Gap Junctions ◽

Ganglion Cell ◽

Dopamine Receptor ◽

Dopamine Release ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Rabbit Retina ◽

Cell Network ◽

Stimulation Of

Many retinal ganglion cells are coupled via gap junctions with neighboring amacrine cells and ganglion cells. We investigated the extent and dynamics of coupling in one such network, the OFF α ganglion cell of rabbit retina and its associated amacrine cells. We also observed the relative spread of Neurobiotin injected into a ganglion cell in the presence of modulators of gap junctional permeability. We found that gap junctions between amacrine cells were closed via stimulation of a D1 dopamine receptor, while the gap junctions between ganglion cells were closed via stimulation of a D2 dopamine receptor. The pairs of hemichannels making up the heterologous gap junctions between the ganglion and amacrine cells were modulated independently, so that elevations of cAMP in the ganglion cell open the ganglion cell hemichannels, while elevations of cAMP in the amacrine cell close its hemichannels. We also measured endogenous dopamine release from an eyecup preparation and found a basal release from the dark-adapted retina of approximately 2 pmol/min during the day. Maximal stimulation with light increased the rate of dopamine release from rabbit retina by 66%. The results suggest that coupling between members of the OFF α ganglion cell/amacrine cell network is differentially modulated with changing levels of dopamine.

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Representations of the amacrine cell population underlying retinal motion anticipation

10.1101/830976 ◽

2019 ◽

Author(s):

Michael D. Menz ◽

Dongsoo Lee ◽

Stephen A. Baccus

Keyword(s):

Ganglion Cell ◽

Cell Population ◽

Amacrine Cell ◽

Ganglion Cells ◽

Computational Modelling ◽

Amacrine Cells ◽

Cell Populations ◽

Population Activity ◽

General Role ◽

Moving Stimuli

AbstractRetinal amacrine cells are a diverse population of inhibitory interneurons, posing a challenge to understand the specific roles of those interneurons in computations of the similarly diverse ganglion cell population. Here we study the predictive computation of motion anticipation, which is thought to compensate for processing delays when encoding moving objects. We recorded the membrane potential of the salamander amacrine cell population optically while recording electrically from ganglion cells with a multielectrode array. We find unexpectedly that ganglion cells with the greatest anticipation for moving stimuli exhibit a new type of predictive motion anticipation that is inconsistent with prior models of delayed inhibition. Based on the spatiotemporal correlations between thousands of amacrine and ganglion cell pairs, we modeled the contribution of the traveling wave of activity for different amacrine cell populations to the encoding of a moving bar. These models indicate that the population responses of slow biphasic amacrine cells create the greatest contribution to both types of ganglion cell motion anticipation, supporting a role for this specific amacrine cell class in the predictive encoding of moving stimuli.Significance StatementThe prediction of moving stimuli is a widespread function occurring in both visual and auditory systems. The diversity of interneuron populations makes it a challenge to understand the mechanisms of these computations. To analyze how the retina anticipates motion, we optically measured inhibitory amacrine cell population activity simultaneously with electrical recording from ganglion cell populations. We then used computational modelling to assess which amacrine cell types have the right spatiotemporal responses to generate motion anticipation. In contrast to previous suggestions of a general role for inhibition, we find that slow biphasic amacrine cells specifically have the greatest contribution to motion anticipation, thus highlighting the need to directly measure and model the effects of interneuron populations in complex sensory computations.

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Amacrine cell contributions to red-green color opponency in central primate retina: A model study

Visual Neuroscience ◽

10.1017/s0952523807070502 ◽

2007 ◽

Vol 24 (4) ◽

pp. 535-547 ◽

Cited By ~ 3

Author(s):

D.S. LEBEDEV ◽

D.W. MARSHAK

Keyword(s):

Amacrine Cell ◽

Ganglion Cells ◽

Receptive Fields ◽

Amacrine Cells ◽

Bipolar Cells ◽

Cone Mosaic ◽

Model Study ◽

Cone Type ◽

Color Opponency ◽

Activity Dependent

To investigate the contributions of amacrine cells to red-green opponency, a linear computational model of the central macaque retina was developed based on a published cone mosaic. In the model, amacrine cells of ON and OFF types received input from all neighboring midget bipolar cells of the same polarity, but OFF amacrine cells had a bias toward bipolar cells whose center responses were mediated by middle wavelength sensitive cones. This bias might arise due to activity dependent plasticity because there are midget bipolar cells driven by short wavelength sensitive cones in the OFF pathway. The model midget ganglion cells received inputs from neighboring amacrine cells of both types. As in physiological experiments, the model ganglion cells showed spatially opponent responses to achromatic stimuli, but they responded to cone isolating stimuli as though center and surround were each driven by a single cone type. Without amacrine cell input, long and middle wavelength sensitive cones contributed to both the centers and surrounds of model ganglion cell receptive fields. According to the model, the summed amacrine cell input was red-green opponent even though inputs to individual amacrine cells were unselective. A key prediction is that GABA and glycine depolarize two of the four types of central midget ganglion cells; this may reflect lower levels of the potassium chloride co-transporter in their dendrites.

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The photoresponses of structurally identified amacrine cells in the turtle retina

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

10.1098/rspb.1982.0019 ◽

1982 ◽

Vol 214 (1196) ◽

pp. 403-415 ◽

Cited By ~ 24

Keyword(s):

Time Course ◽

Amacrine Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Homogeneous Distribution ◽

Inner Plexiform Layer ◽

Intracellular Recordings ◽

Cell Processes ◽

Layer I

Intracellular recordings were obtained from amacrine cells afterwards identified morphologically by horseradish peroxidase injection. There is a correlation between the time course of the photoresponses and the distribution of the cell processes across the inner plexiform layer (i. p. l.). Cells producing the shortest duration, transient ‘on‒off’ photoresponses branched in a single, narrow stratum of the i. p. l. (3‒7 μm across). Transient photoresponses with a longer time course were recorded from cells branching in a thicker stratum of i. p. l. (up to 20 μm), or from bistratified cells. Amacrine cells producing sustained centre-on or centre-off photoresponses were radially diffused across the whole i. p. l.; therefore this type of photoresponse need not be associated with a specific cellular stratification within the i. p. l. It is concluded that the two main functional types of amacrine cell, i. e. transient on‒off and sustained centre-on and centre-off, are subject to different structural organization of inputs than are the homologous physiological types of ganglion cells in this species, in the cat and in the carp. In a summary diagram the observed characteristics of the photoresponses are tentatively explained in term s of a non-homogeneous distribution of bipolar synaptic inputs along amacrine cell processes.

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