Interactions of Inhibition and Excitation in the Light-Evoked Currents of X Type Retinal Ganglion Cells

1998 ◽  
Vol 80 (6) ◽  
pp. 2975-2990 ◽  
Author(s):  
Ethan D. Cohen

Cohen, Ethan D. Interactions of inhibition and excitation in the light-evoked currents of X type retinal ganglion cells. J. Neurophysiol. 80: 2975–2990, 1998. The excitatory and inhibitory conductances driving the light-evoked currents (LECs) of cat and ferret on- and off-center X ganglion cells were examined in sliced and isolated retina preparations using center spot stimulation in tetrodotoxin (TTX)-containing Ringer. on-center X ganglion cells showed an increase in an excitatory conductance reversed positive to +20 mV during the spot stimulus. At spot offset, a transient inhibitory conductance was activated on many cells that reversed near E Cl. off-center X ganglion cells showed increases in a sustained inhibitory conductance that reversed near E Cl during spot stimulation. At spot offset, an excitatory conductance was activated that reversed positive to +20 mV. The light-evoked current kinetics of on- and off-center X cells to spot stimulation did not significantly differ in form from their Y cell counterparts in TTX Ringer. When inhibition was blocked, current-voltage relations of the light-evoked excitatory postsynaptic currents (EPSCs) of both on- and off-X cells were L-shaped and reversed near 0 mV. The EPSCs averaged between 300 and 500 pA at −80 mV. The metabotropic glutamate receptor agonist 2-amino-4-phosphonobutyric acid (APB), was used to block on-center bipolar cell function. The LECs of on-X ganglion cells were totally blocked in APB at all holding potentials. APB caused prominent reductions in the dark holding current and synaptic noise of on-X cells. In contrast, the LECs of off-X ganglion cells remained in APB. An increase in the dark holding current was observed. The excitatory amino acid receptor antagonist combination of d-amino-5-phosphono-pentanoic acid (d-AP5) and 2,3-dihydroxy-6-nitro-7-sulfamoyl-benzo-(F)-quinoxalinedione (NBQX) was used to block ionotropic glutamate receptor retinal neurotransmission. The LECs of all on-X ganglion cells were totally blocked, and their holding currents were reduced similar to the actions of APB. For off-X ganglion cells, the antagonist combination always blocked the excitatory current at light-off; however, in many cells, the inhibitory current at light-on remained. on-center X ganglion cells receive active excitation during center illumination, and a transient inhibition at light-off. In contrast off-center X ganglion cells experience a sustained active inhibition during center illumination, and a shorter increase in excitation at light-offset. Cone bipolar cells provide a resting level of glutamate release on X ganglion cells on which their light-evoked currents are superimposed.

1989 ◽  
Vol 94 (6) ◽  
pp. 987-995 ◽  
Author(s):  
J B Troy ◽  
C Enroth-Cugell

We examined the dependence of the center radius of X cells on temporal frequency and found that at temporal frequencies above 40 Hz the radius increases in a monotonic fashion, reaching a size approximately 30% larger at 70 Hz. This kind of spatial expansion has been predicted with cable models of receptive fields where inductive elements are included in modeling the neuronal membranes. Hence, the expansion of the center radius is clearly important for modeling X cell receptive fields. On the other hand, we feel that it might be of only minor functional significance, since the responsivity of X cells is attenuated at these high temporal frequencies and the signal-to-noise ratio is considerably worse than at low and midrange temporal frequencies.


1976 ◽  
Vol 68 (4) ◽  
pp. 465-484 ◽  
Author(s):  
A W Kirby ◽  
C Enroth-Cugell

The effects of picrotoxin and bicuculline upon the discharge pattern of center-surround organized cat retinal ganglion cells of X and Y type were studied. All experiments were carried out under scotopic or possibly low mesopic conditions; mostly but not exclusively on-center cells were studied. Stimuli were chosen so that responses were either; (a) "purely" central; (b) surround dominated; or (c) clearly mixed but center dominated. In each case a pre-drug control response was estaboished, the drug was administered intravenously, and its subsequent effect upon the response was observed. In Y cells both picrotoxin and bicucullin caused the center-driven component of the response to become somewhat reduced in magnitude, while the surround component was substantially reduced. There was thus a change in center-surround balance in favor of the center-driven component. Responses of X cells remained virtually unaffected by both picrotoxin and bicuculline.


2014 ◽  
Vol 112 (12) ◽  
pp. 3125-3137 ◽  
Author(s):  
C. Zhang ◽  
S. B. Rompani ◽  
B. Roska ◽  
M. A. McCall

In the central nervous system, inhibition shapes neuronal excitation. In spinal cord glycinergic inhibition predominates, whereas GABAergic inhibition predominates in the brain. The retina uses GABA and glycine in approximately equal proportions. Glycinergic crossover inhibition, initiated in the On retinal pathway, controls glutamate release from presynaptic OFF cone bipolar cells (CBCs) and directly shapes temporal response properties of OFF retinal ganglion cells (RGCs). In the retina, four glycine receptor (GlyR) α-subunit isoforms are expressed in different sublaminae and their synaptic currents differ in decay kinetics. GlyRα1, expressed in both On and Off sublaminae of the inner plexiform layer, could be the glycinergic isoform that mediates On-to-Off crossover inhibition. However, subunit-selective glycine contributions remain unknown because we lack selective antagonists or cell class-specific subunit knockouts. To examine the role of GlyRα1 in direct inhibition in mature RGCs, we used retrogradely transported adeno-associated virus (AAV) that performed RNAi and eliminated almost all glycinergic spontaneous and visually evoked responses in PV5 (OFFαTransient) RGCs. Comparisons of responses in PV5 RGCs infected with AAV-scrambled-short hairpin RNA (shRNA) or AAV- Glra1-shRNA confirm a role for GlyRα1 in crossover inhibition in cone-driven circuits. Our results also define a role for direct GlyRα1 inhibition in setting the resting membrane potential of PV5 RGCs. The absence of GlyRα1 input unmasked a serial and a direct feedforward GABAAergic modulation in PV5 RGCs, reflecting a complex interaction between glycinergic and GABAAergic inhibition.


1979 ◽  
Vol 74 (2) ◽  
pp. 275-298 ◽  
Author(s):  
J D Victor ◽  
R M Shapley

We investigated receptive field properties of cat retinal ganglion cells with visual stimuli which were sinusoidal spatial gratings amplitude modulated in time by a sum of sinusoids. Neural responses were analyzed into the Fourier components at the input frequencies and the components at sum and difference frequencies. The first-order frequency response of X cells had a marked spatial phase and spatial frequency dependence which could be explained in terms of linear interactions between center and surround mechanisms in the receptive field. The second-order frequency response of X cells was much smaller than the first-order frequency response at all spatial frequencies. The spatial phase and spatial frequency dependence of the first-order frequency response in Y cells in some ways resembled that of X cells. However, the Y first-order response declined to zero at a much lower spatial frequency than in X cells. Furthermore, the second-order frequency response was larger in Y cells; the second-order frequency components became the dominant part of the response for patterns of high spatial frequency. This implies that the receptive field center and surround mechanisms are physiologically quite different in Y cells from those in X cells, and that the Y cells also receive excitatory drive from an additional nonlinear receptive field mechanism.


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