Retinal Ganglion Cell Classes in the Old World Monkey: Morphology and Central Projections

Leventhal, Audie G.; Rodieck, R. W.; Dreher, Bogdan

doi:10.1126/science.7268423

Cited by 407 publications

(198 citation statements)

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“…DISCUSSION The results reported here provide additional information about the structural basis for the segregation of function in the LGN of the monkey. In support of previous physiological (3-5, 15, 22) and anatomical studies (13,14,23,24), the present findings demonstrate that the color-coded ganglion cells in the retina project exclusively to the parvocellular geniculate layers, whereas the broad-band cells send their axons to the magnocellular laminae. In addition to their specific destinations, these two classes of optic-tract fibers have structurally distinct arborizations.…”

supporting

confidence: 92%

Retinal afferent arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey.

Michael

1988

Proc. Natl. Acad. Sci. U.S.A.

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Optic tract fibers and cell bodies in the lateral geniculate nucleus of the monkey were studied intracellularly with micropipette electrodes containing the marker enzyme horseradish peroxidase. Single optic-tract fibers always projected to only one of the six geniculate layers. The majority of the axons innervating the four parvocellular laminae were red/green opponent color units; their terminations formed cylindrical columns that were perpendicular to the layers. In similar fashion, the geniculate cells in the parvocellular layers were mostly red/green units with narrow, bipolar dendritic fields oriented normal to the laminar borders. The majority of the retinal axons ending in parvocellular layers 6 and 5 were on-center units; nearly all geniculate cells in these two laminae were also on-center neurons. In layers 4 and 3 most terminating optic-tract fibers, as well as the geniculate cells themselves, were off-center units. AU axons projecting to the magnocellular layers were broad-band units with spherical terminal arborizations. The magnocellular geniculate neurons, which were also broad band, had extensive spherical dendritic fields that often crossed laminar borders. Thus, the terminal patterns of each class of retinogeniculate axon closely resembled the dendritic orientations of the functionally related geniculate target cells.The ganglion cells in the retina of the monkey consist of several distinct functional classes (1). Nearly all of them have on-center or off-center receptive fields. On-center ganglion cells discharge in response to an increase in the illumination falling on their receptive field centers, whereas off-center cells fire when the light level decreases. The field centers of many of these ganglion cells receive input from only one of the three cone classes; in turn, their surrounds are connected with only one of the two remaining cone types. As a result of these synaptic connections, the cells are excited by certain colors and inhibited by others. Some ganglion cells have center/surround receptive fields but show no special interest in color; both their centers and surrounds receive summating inputs from all three cone types. Consequently, these ganglion cells have broad-band spectral sensitivities.Axons of the retinal ganglion cells project to the lateral geniculate nucleus (LGN) in the thalamus. Here are found the same functional classes seen in the retina, with no obvious changes in their physiological properties (2-4). In the retina the different ganglion cell types are often found next to one another, whereas in the LGN each functional class is rather strictly confined to certain layers. For instance, nearly all opponent color neurons are located in the four dorsal parvocellular layers, whereas most broad-band cells are limited to the two ventral magnocellular laminae (2, 4, 5). Within the parvocellular layers almost all neurons in laminae 6 and 5 are on-center cells, whereas layers 4 and 3 contain mostly off-center neurons (4). This laminar separation of the geniculate-cell ...

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supporting

confidence: 92%

Retinal afferent arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey.

Michael

1988

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, lesions of the lingual and caudal fusiform gyri cause cerebral achromatopsia in humans with relative sparing of non-chromatic vision such as motion (Zeki, 1990;Humphreys, 1995). In Old World primates at least motion and colour ⁄ form processing is undertaken by separate, magnocellular and parvocellular neuronal pathways that originate in the retina, which are segregated in the thalamus (Leventhal et al 1981;Livingstone & Hubel, 1988;Maunsell & Gibson, 1992) before reaching specific magnocellular and parvocellular sublayers and modules in the visual cortex (Leventhal et al 1981;Conley & Fitzpatrick, 1989;Merigan et al 1991). The predominant projections from the magnocellular pathway continues dorsally to area MT (V5), the medial superior temporal cortex and on to the posterior parietal cortex (DeYoe & Van Essen, 1988).…”

Section: Parcellation and Connectivity Of The Visual Cortexmentioning

confidence: 99%

Unravelling the development of the visual cortex: implications for plasticity and repair

Bourne

2010

Journal of Anatomy

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The visual cortex comprises over 50 areas in the human, each with a specified role and distinct physiology, connectivity and cellular morphology. How these individual areas emerge during development still remains something of a mystery and, although much attention has been paid to the initial stages of the development of the visual cortex, especially its lamination, very little is known about the mechanisms responsible for the arealization and functional organization of this region of the brain. In recent years we have started to discover that it is the interplay of intrinsic (molecular) and extrinsic (afferent connections) cues that are responsible for the maturation of individual areas, and that there is a spatiotemporal sequence in the maturation of the primary visual cortex (striate cortex, V1) and the multiple extrastriate ⁄ association areas. Studies in both humans and non-human primates have started to highlight the specific neural underpinnings responsible for the maturation of the visual cortex, and how experience-dependent plasticity and perturbations to the visual system can impact upon its normal development. Furthermore, damage to specific nuclei of the visual cortex, such as the primary visual cortex (V1), is a common occurrence as a result of a stroke, neurotrauma, disease or hypoxia in both neonates and adults alike. However, the consequences of a focal injury differ between the immature and adult brain, with the immature brain demonstrating a higher level of functional resilience. With better techniques for examining specific molecular and connectional changes, we are now starting to uncover the mechanisms responsible for the increased neural plasticity that leads to significant recovery following injury during this early phase of life. Further advances in our understanding of postnatal development ⁄ maturation and plasticity observed during early life could offer new strategies to improve outcomes by recapitulating aspects of the developmental program in the adult brain.

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“…Most ganglion cells in the primate retina and its major target, the dorsal lateral geniculate nucleus of the thalamus (LGN), belong to the parvocellular (P) or magnocellular (M) pathway (Leventhal et al 1981). All P-and M-cells show receptive fields of the center-surround type and can be reasonably well characterized by linear models Kaplan 1997a,b, 1999;: each neuron responds as if it computes a weighted sum of the intensity of the pattern imaged on its receptive field.…”

Section: Introductionmentioning

confidence: 99%

Linear and Nonlinear Contributions to the Visual Sensitivity of Neurons in Primate Lateral Geniculate Nucleus

Solomon

Tailby

Cheong

et al. 2010

Journal of Neurophysiology

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Solomon SG, Tailby C, Cheong SK, Camp AJ. Linear and nonlinear contributions to the visual sensitivity of neurons in primate lateral geniculate nucleus. J Neurophysiol 104: 1884 -1898, 2010. First published August 4, 2010 doi:10.1152/jn.01118.2009. Several parallel pathways convey retinal signals to the visual cortex of primates. The signals of the parvocellular (P) and magnocellular (M) pathways are well characterized; the properties of other rarely encountered cell types are distinctive in many ways, but it is not clear that they can provide signals with the same fidelity. Here we study this by characterizing the temporal receptive field of neurons in the lateral geniculate nucleus of anesthetized marmosets. For each neuron, we measured the response to a flickering uniform field, and, from this, estimated the linear and nonlinear receptive fields using spike-triggered average (STA) and spike-triggered covariance (STC) analyses. As expected the response of most P-cells was dominated by the STA, but the response of most M-cells required additional nonlinear components, and these usually acted to suppress cell responses. The STC analysis showed stronger suppressive axes in suppressed-by-contrast cells, and both suppressive and excitatory axes in ON-OFF cells. Together, the STA and the STC analyses form a model of the temporal response to a large uniform field: under this model, the information that was provided by suppressed-by-contrast cells or ON-OFF cells approached that provided by the P-and M-cells. However, whereas Pand M-cells provided more information about luminance, the nonlinear cells provided more information about the contrast energy. This suggests that the nonlinear cells provide complimentary signals to those of P-and M-cells, with reasonably high fidelity, and may play an important role in normal visual processing.

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Retinal Ganglion Cell Classes in the Old World Monkey: Morphology and Central Projections

Cited by 407 publications

References 22 publications

Retinal afferent arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey.

Retinal afferent arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey.

Unravelling the development of the visual cortex: implications for plasticity and repair

Linear and Nonlinear Contributions to the Visual Sensitivity of Neurons in Primate Lateral Geniculate Nucleus

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