scholarly journals Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

2019 ◽  
Author(s):  
Xiaoyang Yao ◽  
Greg D. Field

AbstractInformation about motion is encoded by direction-selective retinal ganglion cells (DSGCs). These cells reliably transmit this information across a broad range of light levels, spanning moonlight to sunlight. Previous work indicates that adaptation to low light levels causes heterogeneous changes to the direction tuning of ON-OFF (oo)DSGCs and suggests that superior-preferring ON-OFF DSGCs (s-DSGCs) are biased toward detecting stimuli rather than precisely signaling direction. Using a large-scale multi-electrode array, we measured the absolute sensitivity of ooDSGCs and found that s-DSGCs are ten-fold more sensitive to dim flashes of light than other ooDSGCs. We measured their receptive field sizes and found that s-DSGCs also have larger receptive fields than other ooDSGCs, however, the size difference does not fully explain the sensitivity difference. Using a conditional knockout of gap junctions and pharmacological manipulations, we demonstrate that GABA-mediated inhibition contributes to the difference in absolute sensitivity and receptive field size at low light levels, while the connexin36-mediated gap junction coupling plays a minor role. We further show that GABA-mediated inhibition masks the OFF response of ooDSGCs under scotopic conditions, restricting their responses to increases in light. These results reveal that GABAergic inhibition controls and differentially modulates the responses of ooDSGCs under scotopic conditions.Significance StatementLight adaptation and parallel processing are two major functions of retina. Here we show that parallel processing is differentially regulated between photopic and scotopic conditions across DSGCs. This differential adaptation alters the absolute sensitivity and RF size of s-DSGCs relative to other ooDSGC types. These results point to novel mechanisms and possibly new circuit elements that shape retinal processing of motion under rod-mediated light levels.

1991 ◽  
Vol 6 (3) ◽  
pp. 271-281 ◽  
Author(s):  
S.L. Pallas ◽  
B.L. Finlay

AbstractUnilateral partial ablation of the superior colliculus in the hamster results in a compression of the retinotopic map onto the remaining tectal fragment. In a previous electrophysiological study (Pallas & Finlay, 1989a), we demonstrated that receptive-field properties of single tectal units (including receptive-field size) remain unchanged, despite the increased afferent/target convergence ratios in the compressed tecta. The present study was done to investigate the mechanism that produces increased convergence from retina to tectum at the population level while maintaining apparent stability of convergence at the single neuron level. We injected comparable quantities of horseradish peroxidase into the tecta of normal adult hamsters and adult hamsters that had received neonatal partial tectal ablations of varying magnitude. We then compared the area of retina backfilled from the injection and the number and density of labeled retinal ganglion cells within it to the size of the remaining tectal fragment.As expected from earlier anatomical (Jhaveri & Schneider, 1974) and physiological (Finlay et al., 1979a; Pallas & Finlay, 1989a) studies demonstrating compression of the retinotectal projection, we found that the area of retina labeled from a single tectal injection site increases linearly with decreasing tectal fragment size. However, for fragment sizes down to 30% of normal, total number of retinal ganglion cells projecting to the injection site remains in or above the normal range. For large lesions (less than 30% of tectum remaining), total number of labeled retinal ganglion cells declines from normal, despite the fact that a larger absolute area of retina is represented on each unit of tectum under these conditions. Comparison of retinal ganglion cell density with tectal fragment size shows an initial decline with decreasing fragment size, which becomes sharper with very large lesions (small tectal fragments).The maintenance of the normal number of retinal ganglion cells innervating each patch of tectum could be accomplished by an elimination of the tectal collaterals of some retinal ganglion cells. Our results suggest that, in addition to collateral elimination, reduction in the size of ganglion cell arbors is occurring, since the peak density of backfilled ganglion cells declines less rapidly than backfilled retinal area increases, especially for small lesions. However, arbor reduction and collateral elimination must occur in such a way that individual tectal cells represent the same amount of visual space as normal.Thus, collateral elimination and arbor reduction are two mechanisms that operate to maintain afferent/target convergence ratios (and thus receptive-field properties) over large variations in afferent availability. This compensation may occur through an activity-dependent stabilization mechanism that does not change its selectivity even when excess afferents are available. For very large lesion sizes, receptive-field size and innervating ganglion cell number and density are not preserved, thus demonstrating a limit to the afferent/target matching mechanism. The same ontogenetic mechanisms might provide a buffer for normal variations in afferent populations, and could help to align topographic maps with differing numbers of afferents.


1996 ◽  
Vol 75 (5) ◽  
pp. 1878-1893 ◽  
Author(s):  
S. A. Bloomfield

1. Intracellular recordings were obtained from 21 amacrine cells and 12 ganglion cells in the isolated, superfused retina-eyecup of the rabbit. Cells were subsequently labeled with horseradish peroxidase (HRP) or N-(2-aminoethyl)-biotinamide hydrochloride (Neurobiotin) for morphologic identification. 2. Initial experiments performed on three amacrine cells and three ganglion cells showed that 1 microM tetrodotoxin (TTX) abolished all spiking. This included both large-amplitude and small-amplitude spikes recorded in many amacrine cells, indicating that they are mediated by voltage-gated sodium channels. 3. The center-receptive-field size of 18 amacrine cells and 9 ganglion cells was measured with the use of a 50-microns-wide/6.0-mm-long rectangular slit of light that was displaced along its minor axis (parallel to the visual streak) in steps as small as 3 microns. The retina was then bathed in 1 microM TTX, or individual cells were injected with 50 mM QX-314, a quatemary lidocaine derivative, to abolish all spiking, and the center-receptive field of each cell was then remeasured. 4. Although TTX blocked spiking in all ganglion cells (dendritic diameters ranging from 302 to 969 microns), it produced no significant change in the size of their center-receptive fields. This finding argues that passive, electrotonic spread of synaptic inputs to ganglion cell dendritic arbors is adequate for efficient propagation from terminal branches to the soma; active propagation via voltage-gated sodium channels plays no apparent role. 5. In contrast, TTX and QX-314 had variable effect on the receptive fields of amacrine cells, which was related to the size of their dendritic arbors. Whereas TTX had no significant effect on the receptive-field size of amacrine cells whose dendritic arbors were < 525 microns across, the center-receptive fields of larger amacrine cells were reduced, on average, by 40%; QX-314 produced a very similar average reduction of 39%. Moreover, for these larger cells, there was a direct relationship between the magnitude of the reduction in receptive-field size produced by TTX or QX-314 and the size of a cell's dendritic arbor. This relationship was true whether the change in receptive-field size was measured in absolute terms or as percent reduction from control values. 6. Interestingly, TTX and QX-314 also significantly reduced the amplitude of slow potentials recorded in amacrine cells by an average of 22 and 24%, respectively. However, the amplitude of slow potentials recorded in ganglion cells were relatively uneffected by TTX. 7. These findings are consistent with the idea that, for amacrine cells with dendritic arbors spanning > 525 microns, active propagation of synaptic signals mediated by voltage-gated sodium channels is necessary for efficient movement of information across a cell's dendritic arbor and thus plays a major role in shaping their receptive fields. Although the TTX effects may also reflect an indirect contribution from altered synaptic input derived from presynaptic spiking neurons, the strong similarity between the effects of TTX and QX-314 argues that any such contribution was minor. For smaller amacrine cells, passive, electrotonic spread of signals appears adequate for efficient propagation within their limited dendritic arbors.


2006 ◽  
Vol 23 (1) ◽  
pp. 137-142 ◽  
Author(s):  
WAYNE MICHAEL KING ◽  
VIMAL SARUP ◽  
YVES SAUVÉ ◽  
COLLEEN M. MORELAND ◽  
DAVID O. CARPENTER ◽  
...  

Glaucoma is a major cause of blindness and is characterized by death of retinal ganglion cells. In a rat model of glaucoma in which intraocular pressure is raised by cautery of episcleral veins, the somata and dendritic arbors of surviving retinal ganglion cells expand. To assess physiological consequences of this change, we have measured visual receptive-field size in a primary retinal target, the superior colliculus. Using multiunit recording, receptive-field sizes were measured for glaucomatous eyes and compared to both those measured for contralateral control eyes and to homolateral eyes of unoperated animals. Episcleral vein occlusion increased intraocular pressure. This was accompanied by a significant increase in receptive-field size across the superior colliculus. The expansion of receptive fields was proportional to both degree and duration of the increase of intraocular pressure. We suggest that this increase in the size of receptive fields of glaucomatous eyes may be related to the increase in the size of dendritic arbors of the surviving ganglion cells in retina.


2005 ◽  
Vol 93 (6) ◽  
pp. 3537-3547 ◽  
Author(s):  
Chong Weng ◽  
Chun-I Yeh ◽  
Carl R. Stoelzel ◽  
Jose-Manuel Alonso

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.


1987 ◽  
Vol 510 (1 Olfaction and) ◽  
pp. 504-505
Author(s):  
CHARLOTTE M. MISTRETTA ◽  
TAKATOSHI NAGAI ◽  
ROBERT M. BRADLEY

2008 ◽  
Vol 25 (4) ◽  
pp. 419-427 ◽  
Author(s):  
Kazunori Yamamoto ◽  
Hiroshi Jouhou ◽  
Masanori Iwasaki ◽  
Akimichi Kaneko ◽  
Masahiro Yamada

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