Research Article
VEP and PERG acuity in anesthetized young adult rhesus monkeys
- JAMES N. VER HOEVE, YURI P. DANILOV, CHARLENE B.Y. KIM, PETER D. SPEAR
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- Published online by Cambridge University Press:
- 01 July 1999, pp. 607-617
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This study used the swept spatial-frequency method to compare retinal and cortical acuity in anesthetized young adult rhesus monkeys. Visual evoked potentials (VEPs) and pattern electroretinographic responses (PERGs) were recorded from 25 monkeys (age range: 4–12 years) anesthetized with a continuous infusion of propofol. The stimuli were temporally countermodulated sine-wave gratings that increased in spatial frequency within a 10.24-s period. All animals were refracted using acuity estimated from the zero micro-volt intercept of the linear regression of evoked potential amplitude on spatial frequency. Average sweep acuities were 23.7 cycles/deg ± 1.5 S.E.M. and 23.1 cycles/deg ± 1.8 S.E.M. for the PERG and VEP, respectively. VEP and PERG acuities were within the range expected based on acuities estimated from behavioral studies in macaques. PERG and VEP acuities were highly correlated (r = 0.90) and equally sensitive to spherical blur. On a subset of animals, test–retest reliability of animals, and interocular correlations, were high (r = 0.87 and r = 0.83, respectively). Increasing propofol dosage 8-fold did not degrade PERG or VEP acuity. This study demonstrates that high spatial-frequency acuities can be rapidly obtained from young adult rhesus monkeys under a wide dose range of propofol anesthesia using the swept spatial-frequency method.
Experimental eye enlargement in mature animals changes the retinal pigment epithelium
- ALISON M. HARMAN, ROBERT HOSKINS, LYN D. BEAZLEY
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- 01 July 1999, pp. 619-628
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Form deprivation has been shown to result in myopia in a number of species such that the eye enlarges if one eye is permanently closed at the time of eye opening. In the quokka wallaby, the eye grows slowly throughout life. After form deprivation, the eye enlarges by 1–1.5 years of age to the size of that in a 4–6-year-old animal and the number of multinucleated retinal pigment epithelial (RPE) cells in the enlarged retina remains much lower than would be expected in eyes of comparable size. Here we have repeated the experiment but examined animals at 4 years of age. The sutured eye grew significantly larger than did its partner. Numbers of RPE cells were comparable between sutured and partner eyes but were lower than in normal animals of similar age. Reductions in RPE cell density were greater in nasal than in dorsal or ventral retina and were not seen in temporal retina. The distribution of multinucleated cells was quite different in the sutured and open eyes. As in normal eyes, partner eyes had most multinucleated cells in ventral retina, while in the sutured eyes such cells were located mainly in the far periphery. In conclusion, the RPE is significantly changed by the eye enlargement process. However, it is not known whether this change results from an active part played by the RPE in the retinal expansion process or whether the changes are simply a result of a passive increase in area of the RPE.
New role for the primate fovea: A retinal excavation determines photoreceptor deployment and shape
- ALAN D. SPRINGER
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- 01 July 1999, pp. 629-636
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In humans, an increasing density of foveal cone photoreceptors occurs slowly over several years after birth, and accounts for a region that subserves high visual acuity. Concurrently, inner retinal cells move centrifugally away from the foveal center. Such developmental rearrangements reflect complex cellular remodeling after the retinal neuronal cells have differentiated and have formed synapses. Explaining foveal morphogenesis is difficult, because differentiated neuronal cells seem incapable of moving actively. Presented here is a biomechanical explanation of how the above events occur. This hypothesis assumes that the cellular movements throughout the retinal layers occur passively as the eye grows and the retina is stretched. Retinal stretch was simulated using virtual engineering models that were analyzed with finite element analysis. A pit combined with retinal stretch causes the retinal layers to deform in a way that accounts for both the centrifugal and centripetal movement of various retinal cell types. Axially directed, tensile forces associated with stretching the retinal tissue surrounding the pit also accounts for the elongated morphology of foveal cone photoreceptors. These simulations suggest that a pit is required for both the centripetal displacement of cone cells toward the center of the fovea, and for the elongated foveal cone morphology. Since the primate fovea may have minimal impact on acuity, its primary role may be to initiate foveal morphogenesis in slowly developing eyes.
Receptive field and orientation scatter studied by tetrode recordings in cat area 17
- P.A. HETHERINGTON, N.V. SWINDALE
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- 01 July 1999, pp. 637-652
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The receptive-field positions and orientation preferences of neurons occupying the same tangential location in visual cortex are thought to be similar but to have an associated random scatter. However, previous estimates of this scatter may have been inflated by the use of subjective plotting methods, sequential recording of single units, and residual eye movements. Here we report measurements of receptive-field position and orientation scatter in cat area 17 made with tetrodes, which were able to simultaneously isolate and record up to 11 nearby neurons (ensembles). We studied 355 units at 72 sites with moving light and dark bars. Receptive-field sizes and positions were estimated by least-squares fitting of Gaussians to response profiles. We found that receptive-field position scatter was about half of the ensemble average receptive-field size. We confirmed previous estimates of orientation scatter, but calculations suggested that much of it may be accounted for by anatomical scatter in the positions of recorded neurons relative to the tetrode in a smooth map. Orientation tuning width was positively correlated with the degree of orientation scatter. Scatter was not independent in the two eyes: deviations from the local mean for both preferred orientation and receptive-field position were correlated although a significant amount of residual inter-ocular orientation and receptive-field position scatter was present. We conclude that cortical maps of orientation and receptive-field position are more ordered than was previously thought, and that random scatter in receptive-field positions makes a relatively small contribution to cortical point image size.
Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina
- DAIYAN XIN, STEWART A. BLOOMFIELD
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- 01 July 1999, pp. 653-665
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We studied the light-evoked responses of AII amacrine cells in the rabbit retina under dark- and light-adapted conditions. In contrast to the results of previous studies, we found that AII cells display robust responses to light over a 6–7 log unit intensity range, well beyond the operating range of rod photoreceptors. Under dark adaptation, AII cells showed an ON-center/OFF-surround receptive-field organization. The intensity–response profile of the center-mediated response component followed a dual-limbed sigmoidal function indicating a transition from rod to cone mediation as stimulus intensities were increased. Following light adaptation, the receptive-field organization of AII cells changed dramatically. Light-adapted AII cells showed both ON- and OFF-responses to stimulation of the center receptive field, but we found no evidence for an antagonistic surround. Interestingly, the OFF-center response appeared first following rapid light adaptation and was then replaced gradually over a 1–4 min period by the emerging ON-center response component. Application of the metabotropic glutamate receptor agonist APB, the ionotropic glutamate blocker CNQX, 8-bromo-cGMP, and the nitric oxide donor SNAP all showed differential effects on the various center-mediated responses displayed by dark- and light-adapted AII cells. Taken together, these pharmacological results indicated that different synaptic circuits are responsible for the generation of the different AII cell responses. Specifically, the rod-driven ON-center responses are apparently derived from rod bipolar cell synaptic inputs, whereas the cone-driven ON-center responses arise from signals crossing the gap junctions between AII cells and ON-center cone bipolar cells. Additionally, the OFF-center response of light-adapted AII cells reflects direct synaptic inputs from OFF-center cone bipolar cells to AII dendritic processes in the distal inner plexiform layer.
Visual cortical simple cells: Who inhibits whom
- ALAN B. SAUL
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- 01 July 1999, pp. 667-673
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Simple cells display a specific adaptation aftereffect when tested with drifting gratings. The onset of the response to each cycle of the grating is delayed after adapting, but the offset is unaffected. Testing with stationary bars whose luminance was modulated in time revealed that aftereffects occur only at certain points in both space and time. The aftereffects seen with moving stimuli were predicted from those seen with stationary stimuli. These adaptation experiments suggest a model that consists of mutually inhibitory simple cells that are in spatiotemporal quadrature. The inhibition is appropriately localized in space and time to create the observed aftereffects. In this model, inhibition onto direction-selective simple cells arises from simple cells with the same preferred direction.
Alcohol does not affect visual contrast gain mechanisms
- PAULINE PEARSON, BRIAN TIMNEY
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- 01 July 1999, pp. 675-680
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It has been suggested that acetylcholine plays a role in contrast discrimination performance and the regulation of visual contrast gain (Smith, 1996). Since alcohol has been shown to reduce levels of acetylcholine and contrast sensitivity, the present study measured the effects of alcohol on contrast discrimination and explored whether the deficits could be explained as a consequence of reduction in contrast gain. Detection thresholds and contrast increment thresholds under placebo and alcohol (0.06% BAC) conditions were measured in six volunteers. Alcohol was found to impair both detection and discrimination of only high spatial frequencies. However, when the base contrasts used in the increment threshold task were equal multiples of detection threshold, no alcohol-induced changes in increment thresholds were obtained at any spatial frequency. We conclude that alcohol impairs contrast discrimination performance but that no change in contrast gain mechanisms need be postulated to account for the data.
Electrophysiological evidence for transient topographic organization of retinotectal projections during optic nerve regeneration in the lizard, Ctenophorus ornatus
- R.V. STIRLING, S.A. DUNLOP, L.D. BEAZLEY
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- 01 July 1999, pp. 681-693
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In the lizard, Ctenophorus ornatus, anatomical studies have revealed that optic axons regenerate to visual centers within 2 months of nerve crush but that, from the outset, the regenerated projections lack topographic order (Beazley et al., 1997; Dunlop et al., 1997b). Here we assess the functional topography of the regenerated retinotectal projections by electrophysiological recording of extracellular multiunit responses to visual stimulation and by observing the lizards' ability to capture live prey. At the completion of the electrophysiology, DiI was applied locally to the retina and the topography of the tectal projection later assessed. Electrophysiology revealed that, at 2–4.2 months, responses were weak and habituated readily; no retinotopic order was detected. Between 4.5–6 months, responses were more reliable and the majority of lizards displayed a crude retinotopic order, especially in the ventro-temporal to dorso-nasal retinal axis. Although responses were variable between 6–9 months, they tended to be more reliable again thereafter. However, from 6–18 months, the projection consistently lacked topography with many retinal regions projecting to each tectal locus. Lizards, including those with electrophysiological evidence of crude retinotopy, were consistently unable to capture live prey using the experimental eye. Labelling with DiI confirmed the absence of anatomical retinotopy throughout. Taken together, the electrophysiological and anatomical data indicate that retinotopically appropriate axon terminals (or parts thereof) are transiently active whilst inappropriately located ones are silent. Presumably in lizard map-making cues fade with time and/or the mechanisms are lacking to stabilize and refine the ephemeral map. Moreover, the transient retinotopy is insufficient for useful visual function.
Development and regulation of substance P expression in neurons of the tadpole optic tectum
- SHICHUN TU, ELIZABETH A. DEBSKI
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- 01 July 1999, pp. 695-705
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Activity-dependent synaptic plasticity is characteristic of developing visual systems. Using the frog retinotectal system, we investigated the extent to which afferent input affects neurotransmitter expression in a target structure. We have concentrated on a particular subpopulation of tectal cells that is immunoreactive to substance P (SP). Early in development, SP expression in tectal neurons was restricted to the anterior lateral region of the tectum. As tadpoles developed, this expression expanded into progressively more posterior and medial regions in a manner that closely followed the gradient of tectal maturation. At all times, however, anterior and lateral tectal regions had a greater percent of SP-like immunoreactive (SP-ir) cells than posterior and medial ones. Horseradish peroxidase (HRP) labeling of the retinal ganglion cell projection in conjunction with SP immunocytochemistry demonstrated that innervation by retinal ganglion cell terminals preceded the expression of SP by tectal cells. This suggested that the optic nerve may influence SP differentiation and/or expression. In support of this idea, transection of the optic nerve resulted in a decrease in SP expression in the deafferented tectal lobe of tadpoles. This result, opposite to that seen previously in the adult, also indicates that optic nerve–dependent regulation of SP expression in the developing and mature systems occurs through different pathways.
Analysis of two types of cone bipolar cells in the retina of a New World monkey, the marmoset, Callithrix jacchus
- XUEGANG LUO, KRISHNA K. GHOSH, PAUL R. MARTIN, ULRIKE GRÜNERT
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- 01 July 1999, pp. 707-719
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Two types of cone bipolar cells, the blue cone bipolar cell and the diffuse bipolar cell (DB3), were labelled immunohistochemically and investigated in the retina of a New World monkey, the marmoset. Blue cone bipolar cells were labelled with an antiserum against cholecystokinin. Short-wavelength-sensitive (SWS) cones were labelled with an antiserum against the SWS cone opsin. The DB3 cells were labelled with antibodies to calbindin. Blue cone bipolar cells in marmoset do not form a regular mosaic but instead follow the random distribution of the SWS cones. Nevertheless, the SWS cone to blue cone bipolar cell connectivity in marmoset is very similar to that previously described for macaque. In contrast to the blue cone bipolar cells, the DB3 cells form a regular mosaic. The synaptic connectivity of DB3 cells in the inner plexiform layer was analyzed. They make output synapses onto ganglion cells and amacrine cells, and gap junctions with each other. Our results provide further evidence for the existence of parallel bipolar cell pathways in the primate retina and support the view that the retinae of Old World and New World primates have common neuronal connectivity. The random distribution of SWS cones and blue cone bipolar cells is an exception to the general rule of a regular mosaic distribution of cell populations in the retina.
Vision in mice with neuronal redundancy due to inhibition of developmental cell death
- VITTORIO PORCIATTI, TOMMASO PIZZORUSSO, LAMBERTO MAFFEI
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- 01 July 1999, pp. 721-726
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Transgenic mice overexpressing bcl-2, due to inhibition of naturally occurring cell death, have much larger brains and optic nerves as compared to wild-type mice. Since developmental cell death is believed to exert a crucial role in establishing the mature neural circuitry and function, we asked the question of whether basic aspects of vision were altered in bcl-2 mice. Local visually evoked potentials (VEPs) in response to patterned stimuli were recorded from the primary visual cortex. The representation of the vertical meridian was displaced by about 15% in the bcl-2 mouse, accounting for brain expansion. However, visual acuity, contrast threshold, and response latency were normal, indicating that compensatory mechanisms can ensure normal basic properties of vision in spite of marked neuronal redundancy.
A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs
- DANIEL G. GREEN, NATALIA V. KAPOUSTA-BRUNEAU
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- 01 July 1999, pp. 727-741
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The origins of the a- and b-wave of the ERG were studied using simultaneous recordings made across the receptor layer and the full thickness of a piece of isolated albino rat retina. An inwardly directed current flowing across the rod outer segments was eliminated from the recording when postsynaptic activity was blocked with cobalt or when current source density measurements were made along the length of the outer segments. Rod photovoltages were inferred by removing extraneous field potentials from the recordings made across the photoreceptor layer. The spatial properties of the photovoltage indicates the responses came from an area about 100 μm in diameter. The glutamate analog, APB, which blocks depolarizing bipolar cells, eliminated the b-wave but left the a-wave unaffected. The ERG component due to depolarizing bipolar cells was inferred by subtracting recordings obtained before and after APB. After treatment with APB a slow component remained. This component was completely blocked by barium (200 μM), which blocks potassium channels on Müller cells. Barium had virtually no effect on low-intensity photovoltages but did affect the amplitude and shape of the saturated responses. Barium increased the amplitude of the component of the ERG which underlies the b-wave. It was concluded that the depolarizing bipolar cells directly generate the b-wave of the ERG.
The contributions of voltage- and time-dependent potassium conductances to the electroretinogram in rabbits
- B. LEI, I. PERLMAN
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- 01 July 1999, pp. 743-754
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The electroretinogram (ERG) is generated by light-induced electrical activity in retinal cells. Since potassium ions and potassium conductances play a major role in determining the membrane potential of cells, changes in these are expected to affect the amplitude and pattern of the ERG. We recorded the ERG responses and the isolated P-III waves of rabbits after intraocular injections of specific blockers for potassium channels. 4-aminopyridine (4-AP) did not cause any noticeable changes in the ERG while tetraethylammonium chloride (TEA) induced time-dependent effects. Short-term (1–2 h) effects were expressed as significant augmentation of the b-wave with little change in the a-wave. At longer periods of follow-up, the a-wave increased in amplitude while the b-wave decreased. TEA augmented the amplitude of the isolated P-III wave. These effects of TEA can be explained by TEA-induced depolarization of the photoreceptors. Cesium ions and barium ions induced substantial augmentation of the b-wave. Barium but not cesium ions reduced the isolated P-III component of the ERG probably by blocking the potassium channels in the Müller cells. The augmentation of the b-wave by both barium or cesium ions is inconsistent with the Müller cells hypothesis for the ERG b-wave.
Cooperative and competitive spatial interactions in motion integration
- JEAN LORENCEAU, LAURE ZAGO
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- 01 July 1999, pp. 755-770
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Recovering the velocity of objects moving in the visual field requires both the integration and segmentation of local neuronal responses elicited by moving stimuli in primary visual cortex. Herein, we investigate the effects of the contrast, density, spatial proximity, spatial frequency, and spatial configuration of component motions on these complementary processes. Measuring the ability of human observers to discriminate the global direction of motion displays composed of spatially distributed patches of drifting gratings whose motion is locally ambiguous, we provide psychophysical evidence that linking component motion across space is facilitated at low contrast and high patch density. Furthermore, direction discrimination depends on the spatial frequency of component gratings and is more accurate for spatial configurations that contain “virtual” L junctions as compared to configurations composed of “virtual” T junctions. We suggest that the conditions yielding global motion coherence can be accounted for by the existence of anisotropic cooperative/competitive, contrast-dependent, long-range interactions among oriented direction-selective units. In addition, we bring evidence that motion segmentation processes rely upon the processing of moving local spatial discontinuities. The results are discussed in the light of recent psychophysical and physiological evidence that long-range excitatory and inhibitory interactions within primary visual cortex modulate perceptual linking.
Gamma-atrial natriuretic peptide 1–25 is found in bipolar cells in turtle and rat retinas
- SILKE HAVERKAMP, HELGA KOLB, TODD A. BLUTE, LUXIANG CAO, WILLIAM D. ELDRED
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- 01 July 1999, pp. 771-779
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Immunocytochemistry was used to reveal a population of bipolar cells that contain γ-atrial natriuretic peptide 1–25 (γ-ANP) in turtle retina. This same antibody was also used in rat retina as a comparative control. The retinas were examined by both conventional light microscopy and confocal microscopy with double-labeling to determine whether protein kinase C-α-like immunoreactivity (PKC-α-LI) was colocalized with the γ-ANP-LI. Some thick sections of turtle retina immunostained with only the γ-ANP antibody were also examined by electron microscopy. In rat, a subpopulation of bipolar cells with axons terminating close to the ganglion cell layer was labeled. Double-labeling experiments indicated that the γ-ANP-LI and PKC-α-LI were colocalized in rat retina, and thus all the bipolar cells with γ-ANP-LI were rod bipolar cells. In turtle, the γ-ANP antibody labeled certain bipolar cells that were characterized by bistratified axon terminals arborizing on the borders of strata S2/3 and S3/4 in the inner plexiform layer (IPL). Double labeling with PKC-α antibody indicated that bipolar cells with γ-ANP-LI were not the same bipolar cell types with PKC-α-LI. Thus, γ-ANP-LI appears to be a new marker for a distinct type of bipolar cell in turtle retina. At the ultrastructural level, the γ-ANP-LI was visible throughout the cytoplasm of the bipolar cells from dendrites to axon terminals. In the outer plexiform layer (OPL), labeled dendrites contacted photoreceptor pedicles almost exclusively at narrow-cleft basal junctions, but infrequently formed the central element at a photoreceptor ribbon synapse. In the IPL, axon terminals with γ-ANP-LI made ribbon synapses onto a combination of amacrine and ganglion cells. Since narrow-cleft basal junctions and photoreceptor ribbon-related junctions are known to be associated with ON-center bipolar cells in turtle, and since the axon terminals of bipolars with γ-ANP-LI stratify primarily in the ON-strata of the IPL, we suggest that these cells are likely to be ON-center cells. It is possible that the γ-ANP may be involved in regulating the activity of Na+/K+ ATPase or in the modulation of cGMP levels.
Experience-dependent development of NMDAR1 subunit expression in the lateral geniculate nucleus
- MARK A. FAVA, KEVIN R. DUFFY, KATHRYN M. MURPHY
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- 01 July 1999, pp. 781-789
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Monocular deprivation early in postnatal development leads to anatomical and physiological changes in the lateral geniculate nucleus (LGN) and visual cortex. Many of these changes are dependent upon activation of the NMDA receptor. We have examined the role of visual experience in modifying NMDAR1 subunit expression in the LGN of animals reared with various forms of visual deprivation. Following monocular deprivation initiated either at eye opening or at the peak of the critical period, there were approximately 20% fewer NMDAR1-immunopositive neurons in the deprived laminae of the LGN. The loss of NMDAR1-immunopositive neurons was found throughout both the binocular and monocular segments of the LGN and after monocular deprivation until just 3 weeks of age. These results indicate that the loss of NMDAR1 in the LGN following monocular deprivation does not simply reflect changes in the visual cortex. The loss of NMDAR1 expression was not necessarily permanent. Initiation of binocular vision at the peak of the critical period ameliorated the effect of monocular deprivation and the introduction of a period of reverse occlusion led to a complete reversal. Taken together, the results show that the expression of the NMDAR1 subunit in the LGN can be modified by the pattern of visual experience during postnatal development.
Synaptic connectivity of two types of recoverin-labeled cone bipolar cells and glutamic acid decarboxylase immunoreactive amacrine cells in the inner plexiform layer of the rat retina
- MYUNG-HOON CHUN, IN-BEOM KIM, SU-JA OH, JIN-WOONG CHUNG
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- 01 July 1999, pp. 791-800
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We investigated the synaptic connectivity of two populations of recoverin-labeled bipolar cells and GABAergic neurons in the inner plexiform layer (IPL) of the rat retina. Two types of cone bipolar cells, type 2 and type 8, were stained with anti-recoverin antibodies, and GABAergic neurons were stained with anti-glutamic acid decarboxylase (GAD) antibodies. Type 2 cone bipolar axons received synaptic input from amacrine cell processes in 177 cases; among these amacrine cell processes, 92 processes (52.0%) were GAD-like immunoreactive. A total of 159 amacrine cell processes, which are presynaptic to type 8 cone bipolar cells, were observed. Among these processes, 117 processes (73.6%) were GAD-like immunoreactive. The postsynaptic elements at the ribbon synapses of recoverin-labeled cone bipolar cells were observed in 482 processes. In both type 2 and type 8 cone bipolar cells, the major output was to amacrine cell processes. At the ribbon synapses of the type 2 cone bipolar cells, 224 of the postsynaptic profiles were amacrine cell processes, 97 processes (43.3%) were GAD-like immunoreactive. In type 8 cone bipolar cells, 45 processes (30.2%) of 149 amacrine cell processes were GAD-like immunoreactive. Our results provide morphological evidence that GABA is a major transmitter involved in the visual processing of type 2 and 8 cone bipolar cells and GABA may have a stronger influence on type 8 cone bipolar cells than type 2 cone bipolar cells in the IPL of the rat retina.