scholarly journals Representations of the amacrine cell population underlying retinal motion anticipation

2019 ◽  
Author(s):  
Michael D. Menz ◽  
Dongsoo Lee ◽  
Stephen A. Baccus

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.

2010 ◽  
Vol 103 (1) ◽  
pp. 25-37 ◽  
Author(s):  
Erika D. Eggers ◽  
Peter D. Lukasiewicz

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.


2018 ◽  
Author(s):  
Robert E. Marc ◽  
Crystal Sigulinsky ◽  
Rebecca L. Pfeiffer ◽  
Daniel Emrich ◽  
James R. Anderson ◽  
...  

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.


2019 ◽  
Vol 36 ◽  
Author(s):  
Andrea S. Bordt ◽  
Diego Perez ◽  
Luke Tseng ◽  
Weiley Sunny Liu ◽  
Jay Neitz ◽  
...  

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.


2007 ◽  
Vol 24 (4) ◽  
pp. 593-608 ◽  
Author(s):  
STEPHEN L. MILLS ◽  
XIAO-BO XIA ◽  
HIDEO HOSHI ◽  
SALLY I. FIRTH ◽  
MARGARET E. RICE ◽  
...  

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.


2021 ◽  
Vol 38 ◽  
Author(s):  
Xiwu Zhao ◽  
Kwoon Y. Wong

Abstract Intrinsically photosensitive retinal ganglion cells (ipRGCs) signal not only anterogradely to drive behavioral responses, but also retrogradely to some amacrine interneurons to modulate retinal physiology. We previously found that all displaced amacrine cells with spiking, tonic excitatory photoresponses receive gap-junction input from ipRGCs, but the connectivity patterns and functional roles of ipRGC-amacrine coupling remained largely unknown. Here, we injected PoPro1 fluorescent tracer into all six types of mouse ipRGCs to identify coupled amacrine cells, and analyzed the latter’s morphological and electrophysiological properties. We also examined how genetically disrupting ipRGC-amacrine coupling affected ipRGC photoresponses. Results showed that ipRGCs couple with not just ON- and ON/OFF-stratified amacrine cells in the ganglion-cell layer as previously reported, but also OFF-stratified amacrine cells in both ganglion-cell and inner nuclear layers. M1- and M3-type ipRGCs couple mainly with ON/OFF-stratified amacrine cells, whereas the other ipRGC types couple almost exclusively with ON-stratified ones. ipRGCs transmit melanopsin-based light responses to at least 93% of the coupled amacrine cells. Some of the ON-stratifying ipRGC-coupled amacrine cells exhibit transient hyperpolarizing light responses. We detected bidirectional electrical transmission between an ipRGC and a coupled amacrine cell, although transmission was asymmetric for this particular cell pair, favoring the ipRGC-to-amacrine direction. We also observed electrical transmission between two amacrine cells coupled to the same ipRGC. In both scenarios of coupling, the coupled cells often spiked synchronously. While ipRGC-amacrine coupling somewhat reduces the peak firing rates of ipRGCs’ intrinsic melanopsin-based photoresponses, it renders these responses more sustained and longer-lasting. In summary, ipRGCs’ gap junctional network involves more amacrine cell types and plays more roles than previously appreciated.


2002 ◽  
Vol 19 (3) ◽  
pp. 299-305 ◽  
Author(s):  
DAVID W. MARSHAK ◽  
ELIZABETH S. YAMADA ◽  
ANDREA S. BORDT ◽  
WENDY C. PERRYMAN

A labeled ON parasol ganglion cell from a macaque retina was analyzed in serial, ultrathin sections. It received 13% of its input from diffuse bipolar cells. These directed a large proportion of their output to amacrine cells but received a relatively small proportion of their amacrine cell input via feedback synapses. In these respects, they were similar to the DB3 bipolar cells that make synapses onto OFF parasol cells. Bipolar cell axons that contacted the ON parasol cell in stratum 4 of the inner plexiform layer always made synapses onto the dendrite, and therefore, the number of bipolar cell synapses onto these ganglion cells could be estimated reliably by light microscopy in the future. Amacrine cells provided the majority of inputs to the ON parasol cell. Only a few of the presynaptic amacrine cell processes received inputs from the same bipolar cells as the parasol cells, and most of the presynaptic amacrine cell processes did not receive any inputs at all within the series. These findings suggest that most of the inhibitory input to the ON parasol cell originates from other areas of the retina. Amacrine cells presynaptic to the parasol ganglion cell interacted very infrequently with other neurons in the circuit, and therefore, they would be expected to act independently, for the most part.


1993 ◽  
Vol 10 (5) ◽  
pp. 887-897 ◽  
Author(s):  
L. C. L. Silveira ◽  
V. H. Perry ◽  
E. S. Yamada

AbstractThe distribution of ganglion cells and displaced amacrine cells was determined in whole-mounted Aotus retinae. In contrast to diurnal simians, Aotus has only a rudimentary fovea. Ganglion cell density decreases towards the periphery at approximately the same rate along all meridians, but is 1.2–1.8 times higher in the nasal periphery when compared to temporal region at the same eccentricities. The total number of ganglion cells varied from 421,500 to 508,700. Ganglion cell density peaked at 15,000/mm2 at 0.25 mm dorsal to the fovea. The displaced amacrine cells have a shallow density gradient, their peak density in the central region is about 1500–2000/mm2 and their total number varied from 315,900 to 482,800. Comparison between ganglion cell density and areal cortical magnification factor for the primary visual cortex, area 17, shows that there is not a simple proportional representation of the ganglion cell distribution. There is an overrepresentation of the central 10 deg of the visual field in the visual cortex. The present results for Aotus and the results of a similar analysis of data from other primates indicate that the overrepresentation of the central visual field is a general feature of the visual system of primates.


2001 ◽  
Vol 18 (4) ◽  
pp. 559-570 ◽  
Author(s):  
B.E. REESE ◽  
M.A. RAVEN ◽  
K.A. GIANNOTTI ◽  
P.T. JOHNSON

The present study has examined the emergence of cholinergic stratification within the developing inner plexiform layer (IPL), and the effect of ablating the cholinergic amacrine cells on the formation of other stratifications within the IPL. The population of cholinergic amacrine cells in the ferret's retina was identified as early as the day of birth, but their processes did not form discrete strata until the end of the first postnatal week. As development proceeded over the next five postnatal weeks, so the positioning of the cholinergic strata shifted within the IPL toward the outer border, indicative of the greater ingrowth and elaboration of processes within the innermost parts of the IPL. To examine whether these cholinergic strata play an instructive role upon the development of other stratifications which form within the IPL, one-week-old ferrets were treated with l-glutamate in an attempt to ablate the population of cholinergic amacrine cells. Such treatment was shown to be successful, eliminating all of the cholinergic amacrine cells as well as the alpha retinal ganglion cells in the central retina. The remaining ganglion cell classes as well as a few other retinal cell types were partially reduced, while other cell types were not affected, and neither retinal histology nor areal growth was compromised in these ferrets. Despite this early loss of the cholinergic amacrine cells, which are eliminated within 24 h, other stratifications within the IPL formed normally, as they do following early elimination of the entire ganglion cell population. While these cholinergic amacrine cells are present well before other cell types have differentiated, apparently neither they, nor the ganglion cells, play a role in determining the depth of stratification for other retinal cell types.


2011 ◽  
Vol 28 (3) ◽  
pp. 193-204 ◽  
Author(s):  
XIN CHEN ◽  
HAIN ANN HSUEH ◽  
FRANK S. WERBLIN

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.


Development ◽  
1998 ◽  
Vol 125 (6) ◽  
pp. 1059-1066 ◽  
Author(s):  
D.K. Waid ◽  
S.C. McLoon

The different retinal cell types arise during vertebrate development from a common pool of progenitor cells. The mechanisms responsible for determining the fate of individual retinal cells are, as yet, poorly understood. Ganglion cells are one of the first cell types to be produced in the developing vertebrate retina and few ganglion cells are produced late in development. It is possible that, as the retina matures, the cellular environment changes such that it is not conducive to ganglion cell determination. The present study showed that older retinal cells secrete a factor that inhibits the production of ganglion cells. This was shown by culturing younger retinal cells, the test population, adjacent to various ages of older retinal cells. Increasingly older retinal cells, up to embryonic day 9, were more effective at inhibiting production of ganglion cells in the test cell population. Ganglion cell production was restored when ganglion cells were depleted from the older cell population. This suggests that ganglion cells secrete a factor that actively prevents cells from choosing the ganglion cell fate. This factor appeared to be active in medium conditioned by older retinal cells. Analysis of the conditioned medium established that the factor was heat stable and was present in the <3 kDa and >10 kDa fractions. Previous work showed that the neurogenic protein, Notch, might also be active in blocking production of ganglion cells. The present study showed that decreasing Notch expression with an antisense oligonucleotide increased the number of ganglion cells produced in a population of young retinal cells. Ganglion cell production, however, was still inhibited in cultures using antisense oligonucleotide to Notch in medium conditioned by older retinal cells. This suggests that the factor secreted by older retinal cells inhibits ganglion cell production through a different pathway than that mediated by Notch.


Sign in / Sign up

Export Citation Format

Share Document