NMDA and non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus

1991 ◽  
Vol 66 (2) ◽  
pp. 414-428 ◽  
Author(s):  
Y. H. Kwon ◽  
M. Esguerra ◽  
M. Sur

1. We have examined the effects of iontophoresing specific antagonists to excitatory amino acid receptors on the visual responses of cells in lamina A or A1 of the cat's lateral geniculate nucleus (LGN). 2. Cells were classified as On- or Off-center, X or Y, and lagged or nonlagged. The effects of antagonists were studied while cells were stimulated with spots of the appropriate contrast covering the receptive-field center. 3. The N-methyl-D-aspartate (NMDA) receptor antagonists D-2-amino-5-phosphonovaleric acid (D-APV) and 3-(+/-)-2-carboxypiperazin-4-yl)- propyl-1-phosphonic acid (CPP), when iontophoresed at doses that specifically antagonized NMDA-induced responses but not kainate-induced responses, reduced the responses of all cell types in the LGN, including X and Y cells, lagged and nonlagged cells, and On- and Off-center cells. 4. The non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), when applied at doses that specifically antagonized kainate-induced responses but not NMDA-induced responses, also reduced the visual responses of each of the cell types in the LGN. 5. We analyzed quantitatively the effects of D-APV and CNQX on LGN cells. D-APV reduced the responses of lagged cells to a greater extent than the responses of nonlagged cells. CNQX reduced the responses of lagged and nonlagged cells to a similar extent. There was no difference in the effect of D-APV or of CNQX on X and Y cells or on On- and Off-center cells. 6. We analyzed the effects of the antagonists on separate components of responses, including an early component comprising the first 100 ms of response and a late component comprising the next 300 ms of response. D-APV reduced the late component of lagged cell responses to a greater extent than either the early component of the same cells or the early or late component of nonlagged cells. CNQX had nearly equivalent effects on both response components of all cell types. 7. These data indicate that NMDA and non-NMDA receptors make similar contributions to the responses of On- and Off-center and X and Y cells in the LGN. Lagged and nonlagged cells are not differentiated with respect to the contribution of non-NMDA receptors to their visual responses. The greater contribution of NMDA receptors to the responses of lagged cells is consistent with the large contribution made by these receptors to the late response components of lagged cells.(ABSTRACT TRUNCATED AT 250 WORDS)

1990 ◽  
Vol 63 (2) ◽  
pp. 347-355 ◽  
Author(s):  
A. M. Sillito ◽  
P. C. Murphy ◽  
T. E. Salt ◽  
C. I. Moody

1. We have examined the possibility that N-methyl-D-aspartate (NMDA) receptors may be involved in the visual response of relay cells in the cat dorsal lateral geniculate nucleus (dLGN). The selective NMDA receptor antagonists D-2-amino-5-phosphonovalerate (APV) and 3-[(+/-)-2-carboxypiperazin-4-yl]-propyl-1-phosphonic acid (CPP) have been iontophoretically applied to X and Y cells in the dLGN and their effects on the visual response to a light spot flashed within the receptive field center determined. 2. The antagonist effects were assessed at ejection current levels producing a selective blockade of the responses to iontophoretically applied NMDA with respect to those elicited by the non-NMDA receptor agonists quisqualate and kainate. These selective effects were determined in an experimental paradigm where the visual response and responses to NMDA and the non-NMDA receptor agonists were compared in the same test run. The data refer to a total population of 52 cells (28 X, 24 Y). 3. Application of APV abolished or greatly reduced the visual responses of both X and Y cells. The mean percentage reduction in the visual response for the X cells studied was 59 +/- 10% (SE; n = 7) and for the Y cells 66 +/- 8% (SE; n = 11). Both the early onset transient and the sustained component of the visual response to the flashed stimulus were equally affected. 4. The antagonist CPP produced a similar pattern of effect to APV, substantially reducing or abolishing the visual response in both X and Y cells.(ABSTRACT TRUNCATED AT 250 WORDS)


1990 ◽  
Vol 63 (6) ◽  
pp. 1347-1360 ◽  
Author(s):  
P. Heggelund ◽  
E. Hartveit

1. Synaptic mechanisms that might explain the functional properties of the recently discovered class of lagged cells in the dorsal lateral geniculate nucleus (LGN) were analyzed with electrophysiological and pharmacologic techniques. To study the type of excitatory amino acid (EAA) receptor that mediates visual responses of lagged cells, we recorded the response of single cells to a stationary flashing light spot before, during, and after microiontophoretic application of antagonists and agonists to EAA receptors. 2. The visual response of the lagged cells could be almost completely blocked by an antagonist to the N-methyl-D-aspartate (NMDA) receptor. The degree of suppression was dose dependent, and the average maximum degree of suppression for all the cells was 94%. NMDA enhanced the response, and this enhancement was antagonized by NMDA antagonists. A quisqualate/kainate receptor antagonist had no significant effect on the lagged cells. 3. These findings indicate that the visual response in lagged cells is dependent upon activation of NMDA receptors, which may directly result from activation of retinal inputs. 4. No pharmacologic difference was seen between lagged X- and Y-cells, or between lagged ON- and OFF-center cells. 5. gamma-Aminobutyric acid-A (GABA-A) receptor antagonists were used to study whether the characteristic lag of the visual response and the suppression of the initial transient response component of the lagged cells are dependent on geniculate inhibition. Beside enhancement of the visual response, the GABA antagonists strongly reduced the lag of the visual response, and an initial transient response component occurred instead of the initial suppression. The lag remained slightly longer than for nonlagged cells, and the peak firing rate of the transient was below values typical for nonlagged cells, indicating that the lagged cell properties are dependent on other factors beside GABA-A receptor-mediated inhibition. 6. The enhanced visual response during iontophoresis of GABA antagonists could be completely blocked by simultaneous iontophoresis of an NMDA-receptor antagonist. This gives further support to the hypothesis that the retinal input to these cells is mediated by NMDA receptors. 7. The NMDA-receptor/ionophore complex mediates excitatory postsynaptic potentials (EPSPs) characterized by slow rise and decay times and long duration. The ionophore is characterized by a voltage-dependent blockade that makes these receptors particularly sensitive to inhibitory input. The temporal interplay between the slow NMDA receptor-mediated EPSPs and the fast GABA receptor-mediated inhibitory postsynaptic potentials (IPSPs) may explain the characteristic response properties of the lagged cells.


1990 ◽  
Vol 64 (1) ◽  
pp. 206-224 ◽  
Author(s):  
A. B. Saul ◽  
A. L. Humphrey

1. It has recently been shown that the X- and Y-cell classes in the A-layers of the cat lateral geniculate nucleus (LGN) are divisible into lagged and nonlagged types. We have characterized the visual response properties of 153 cells in the A-layers to 1) reveal response features that are relevant to the X/Y and lagged/nonlagged classification schemes, and 2) provide a systematic description of the properties of lagged and nonlagged cells as a basis for understanding mechanisms that affect these two groups. Responses to flashing spots and drifting gratings were measured as the contrast and spatial and temporal modulation were varied. 2. X- and Y-cells were readily distinguished by their spatial tuning. Y-cells had much lower preferred spatial frequencies and spatial resolution than X-cells. Within each functional class (X or Y), however, lagged and nonlagged cells were similar in their spatial response properties. Thus the lagged/nonlagged distinction is not one related to the spatial domain. 3. In the temporal domain X- and Y-cells showed little difference in temporal tuning, whereas lagged and nonlagged cells showed distinctive response properties. The temporal tuning functions of lagged cells were slightly shifted toward lower frequencies with optimal temporal frequencies of lagged X-cells averaging an octave lower than those of nonlagged X-cells. Temporal resolution was much lower in lagged X- and Y-cells than in their nonlagged counterparts. 4. The most dramatic differences between lagged and nonlagged cells appeared in the timing of their responses, as measured by the phase of the response relative to the sinusoidal luminance modulation of a spot centered in the receptive field. Response phase varied approximately linearly with temporal frequency. The slope of the phase versus frequency line is a measure of total integration time, which we refer to as visual latency. Lagged cells has much longer latencies than nonlagged cells. 5. The intercept of the phase versus frequency line is a measure of when in the stimulus cycle the cell responds: we refer to this as the intrinsic or absolute phase of the cell. This measure of response timing not only distinguished lagged and nonlagged cells well but also covaried with the sustained or transient nature of cells' responses to flashed stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)


2011 ◽  
Vol 28 (5) ◽  
pp. 403-417 ◽  
Author(s):  
WALTER F. HEINE ◽  
CHRISTOPHER L. PASSAGLIA

AbstractThe rat is a popular animal model for vision research, yet there is little quantitative information about the physiological properties of the cells that provide its brain with visual input, the retinal ganglion cells. It is not clear whether rats even possess the full complement of ganglion cell types found in other mammals. Since such information is important for evaluating rodent models of visual disease and elucidating the function of homologous and heterologous cells in different animals, we recorded from rat ganglion cells in vivo and systematically measured their spatial receptive field (RF) properties using spot, annulus, and grating patterns. Most of the recorded cells bore likeness to cat X and Y cells, exhibiting brisk responses, center-surround RFs, and linear or nonlinear spatial summation. The others resembled various types of mammalian W cell, including local-edge-detector cells, suppressed-by-contrast cells, and an unusual type with an ON–OFF surround. They generally exhibited sluggish responses, larger RFs, and lower responsiveness. The peak responsivity of brisk-nonlinear (Y-type) cells was around twice that of brisk-linear (X-type) cells and several fold that of sluggish cells. The RF size of brisk-linear and brisk-nonlinear cells was indistinguishable, with average center and surround diameters of 5.6 ± 1.3 and 26.4 ± 11.3 deg, respectively. In contrast, the center diameter of recorded sluggish cells averaged 12.8 ± 7.9 deg. The homogeneous RF size of rat brisk cells is unlike that of cat X and Y cells, and its implication regarding the putative roles of these two ganglion cell types in visual signaling is discussed.


Science ◽  
1979 ◽  
Vol 204 (4397) ◽  
pp. 1114-1117 ◽  
Author(s):  
M. Friedlander ◽  
C. Lin ◽  
S. Sherman

1983 ◽  
Vol 50 (1) ◽  
pp. 240-264 ◽  
Author(s):  
S. C. Mangel ◽  
J. R. Wilson ◽  
S. M. Sherman

We measured response properties of X- and Y-cells from laminae A and A1 of the dorsal lateral geniculate nucleus of monocularly lid-sutured cats at 8, 12, 16, 24, and 52-60 wk of age. Visual stimuli consisted of small spots of light and vertically oriented sine-wave gratings counterphased at a rate of 2 cycles/s. In cats as young as 8 wk of age, nondeprived and deprived neurons could be clearly identified as X-cells or Y-cells with criteria previously established for adult animals. Nonlinear responses of Y-cells from 8- and 12-wk-old cats were often temporally labile; that is, the amplitude of the nonlinear response of nondeprived and deprived cells increased or decreased suddenly. A similar lability was not noted for the linear response component. This phenomenon rarely occurred in older cats. At 8 wk of age, Y-cell proportions (number of Y-cells/total number of cells) in nondeprived and deprived A-laminae were approximately equal. By 12 wk of age and thereafter, the proportion of Y-cells in deprived laminae was significantly lower than that in nondeprived laminae. At no age was there a systematic difference in response properties (spatial resolution, latency to optic chiasm stimulation, etc.) for Y-cells between deprived and nondeprived laminae. Spatial resolution, defined as the highest spatial frequency to which a cell would respond at a contrast of 0.6, was similar for nondeprived and deprived X-cells until 24 wk of age. In these and older cats, the mean spatial resolution of deprived X-cells was lower than that of nondeprived X-cells. This difference was noted first for lamina A1 at 24 wk of age and later for lamina A at 52-60 wk of age. The average latency of X-cells to optic chiasm stimulation was slightly greater in deprived laminae than in nondeprived laminae. No such difference was seen for Y-cells. Cells with poor and inconsistent responses were encountered infrequently but were observed far more often in deprived laminae than in nondeprived laminae. Lid suture appears to affect the development of geniculate X- and Y-cells in very different ways. Not only is the final pattern of abnormalities quite different between these cell groups, but the developmental dynamics of these abnormalities also differ.


1992 ◽  
Vol 68 (3) ◽  
pp. 673-691 ◽  
Author(s):  
A. L. Humphrey ◽  
A. B. Saul

1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (XL) and nonlagged X- and Y-cells (XN and YN). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was greater than 50% in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for XN-cells than for YN- and XL-cells, reflecting the relatively higher discharge rate among XN-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among XN- and YN-cells, PB stimulation had no significant effect on these two latencies; among XL-cells, both latencies were reduced by 43 and 35%, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies greater than 60 ms. Despite the reduction among XL-cells in these 2 latencies during PB stimulation, all but 2 of the 40 XL-cells maintained laggedlike latencies. The majority (95%) of XL-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 XL-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting approximately 45 ms after spot onset. During PB stimulation only three cells lost the dip.(ABSTRACT TRUNCATED AT 400 WORDS)


1992 ◽  
Vol 9 (5) ◽  
pp. 515-525 ◽  
Author(s):  
E. Hartveit ◽  
P. Heggelund

AbstractThe response vs. contrast characteristics of different cell classes in the dorsal lateral geniculate nucleus (LGN) were compared. The luminance of a stationary flashing light spot was varied stepwise while the background luminance was constant. Lagged X cells had lower slope of the response vs. contrast curve (contrast gain), and they reached the midpoint of the response range over which the cells' response varied (dynamic response range) at higher contrasts than nonlagged X cells. These results indicated that nonlagged cells are well suited for detection of small contrasts, whereas lagged cells may discriminate between contrasts over a larger range. The contrast gain and the contrast corresponding to the midpoint of the dynamic response range were similar for X and Y cells. The latency to onset and to half-rise of the visual response decreased with increasing contrast, most pronounced for lagged cells. Even at the highest contrasts, the latency of lagged cells remained longer than for nonlagged cells. For many lagged cells, the latency to half-fall decreased with increasing contrast. It is shown that the differences in the response vs. contrast characteristics between lagged and nonlagged X cells in the cat are similar to the differences between the parvocellular and magnocellular neurones in the monkey.


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