The postnatal development of geniculocortical axon arbors in owl monkeys

Pospichal, Marcie W.; Florence, Sherre L.; Kaas, Jon H.

doi:10.1017/s0952523800011123

Cited by 19 publications

(10 citation statements)

References 68 publications

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“…The general pattern of geniculocortical projections from the individual layers of the LGN in owl monkeys has been reported previously Diamond et al, 1985;Pospichal et al, 1994;Casagrande, 1997, 1998). Results show that, in owl monkeys as in other primates, M LGN axons terminate primarily within cortical layers IV␣ and VI, and K axons terminate within the CO blobs of layers III and in layer I of V1.…”

Section: Injection Sites and Cortical Projections Of The M And P Lgn supporting

confidence: 71%

“…Because M and P LGN cell axons have been found to project exclusively to IV␣ and IV␤, respectively Diamond et al, 1985;Pospichal et al, 1994;Casagrande, 1997, 1998), iontophoretic injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were made into M and P LGN layers in the same animal. Detailed data on synaptic circuits of K LGN axons in V1 were obtained from the same cases used in a previous study (Ding and Casagrande, 1998).…”

Section: Methodsmentioning

confidence: 99%

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Neurochemical comparison of synaptic arrangements of parvocellular, magnocellular, and koniocellular geniculate pathways in owl monkey (Aotus trivirgatus) visual cortex

Shostak

Ding

Casagrande

2002

J of Comparative Neurology

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As in other primates, the lateral geniculate nucleus (LGN) of owl monkeys contains three anatomically and physiologically distinct relay cell classes, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. M and P LGN cells send axons to the upper and lower tiers of layer IV, and K cells send axons to the cytochrome oxidase (CO) blobs of layer III and to layer I of primary visual cortex (V1). Our objective was to compare the synaptic arrangements made by these axon classes. M, P, and K axons were labeled in adult owl monkeys by means of injections of wheat germ agglutinin-horseradish peroxidase into the appropriate LGN layers. The neurochemical content of both pre- and postsynaptic profiles were identified by postembedding immunocytochemistry for gamma-aminobutyric acid (GABA) and glutamate. Our key finding is that the synaptic arrangements made by M, P, and K axons in owl monkey exhibit more similarities than differences. They are exclusively presynaptic, contain glutamate and form asymmetric synapses mainly with glutamate-positive dendritic spines. The majority of the remaining axons synapse with glutamatergic dendritic shafts. There are also differences between LGN pathways. M and P terminals are significantly larger and more likely to make multiple synapses than K axons, although M and P axons do not differ from each other in either of these characteristics. Of interest, a larger percentage of M and K axons than P axons make synapses with GABAergic dendritic shafts. Cells directly postsynaptic to M and K axons are known to exhibit orientation selectivity and, in some cases, direction selectivity. Cells postsynaptic to P axons do not show these properties, but instead tend to reflect their LGN inputs more faithfully; therefore, it is possible that these physiologic differences seen in the cortical cells postsynaptic to different LGN pathways reflect the differential involvement of inhibitory circuits.

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Section: Injection Sites and Cortical Projections Of The M And P Lgn supporting

confidence: 71%

Section: Methodsmentioning

confidence: 99%

Neurochemical comparison of synaptic arrangements of parvocellular, magnocellular, and koniocellular geniculate pathways in owl monkey (Aotus trivirgatus) visual cortex

Shostak

Ding

Casagrande

2002

J of Comparative Neurology

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“…For such restricted binocular properties to exist, all receptive fields would have to be precisely aligned on the horopter or for some fixed depth from the horopter. This would be an exceptionally difficult challenge for the processes regulating innate neuronal connections and one that is not in agreement with current anatomical findings (Florence and Casagrande, 1990;Pospichal et al, 1994). Even if all V1 units were selective for some range of either crossed or uncrossed disparities, it is unlikely that this situation would prevent stereopsis.…”

Section: Disparity Sensitivity In V1 and The Onset Of Stereopsismentioning

confidence: 71%

Postnatal Development of Binocular Disparity Sensitivity in Neurons of the Primate Visual Cortex

et al. 1997

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In macaque monkeys, the age at which neurons in the primary visual cortex (V1) become sensitive to interocular image disparities, a prerequisite for stereopsis, is a matter of conjecture. To resolve this fundamental issue in binocular vision development, we measured the responsiveness of individual V1 neurons in anesthetized and paralyzed infant monkeys as a function of the relative, interocular, spatial phase of dichoptic sine-wave gratings. We found that an adult-like proportion of units were sensitive to interocular image disparity as early as the sixth postnatal day, several weeks before the onset age for stereopsis in monkeys. The ocular dominance distributions of cells in infant monkeys were also indistinguishable from those of adults. Thus, at or only a few days after birth, V1 neurons are capable of combining neural signals from the two eyes as in adults and are sensitive to interocular image disparities. However, the monocular spatial-frequency response properties of these disparity-sensitive units were immature, and their overall responsiveness was far lower than that in adults. During the first 4 postnatal weeks, both the spatial frequency response properties and the peak response amplitude rapidly improved, which resulted in a corresponding increase in the absolute sensitivity of individual units to interocular disparity. The results demonstrate that early binocular vision development in monkeys is not constrained by a paucity of disparity-sensitive V1 neurons but, instead, by the relative immaturity of the spatial response properties and the overall unresponsiveness of existing disparity-sensitive neurons.

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“…At present, there are no data on the synaptic arrangements made by P and M axons in owl monkeys although the light microscopic structure and distribution of these axons in layer IV is analogous to what has been described in other primates, including macaque monkeys (Kaas et al, 1976;Diamond et al, 1985;Pospichal et al, 1994). Our results show that presynaptic owl monkey K profiles in the CO blobs are consistently immuno-positive for glutamate and make asymmetric (Gray's type I) synapses; no K axon terminal profiles are found to be immuno-positive for GABA.…”

Section: Synaptic Arrangements Made By Lgn Axonsmentioning

confidence: 83%

Synaptic and neurochemical characterization of parallel pathways to the cytochrome oxidase blobs of primate visual cortex

Ding

Casagrande

1998

J. Comp. Neurol.

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The primary visual cortex (V1) of primates is unique in that it is both the recipient of visual signals, arriving via parallel pathways (magnocellular [M], parvocellular [P], and koniocellular [K]) from the thalamus, and the source of several output streams to higher order visual areas. Within this scheme, output compartments of V1, such as the cytochrome oxidase (CO) rich blobs in cortical layer III, synthesize new output pathways appropriate for the next steps in visual analysis. Our chief aim in this study was to examine and compare the synaptic arrangements and neurochemistry of elements involving direct lateral geniculate nucleus (LGN) input from the K pathway with those involving indirect LGN input from the M and P pathways arriving from cortical layer IV. Geniculocortical K axons were labeled via iontophoretic injections of wheat germ agglutinin-horseradish peroxidase into the LGN and intracortical layer IV axons (indirect P and M pathways to the CO-blobs) were labeled by iontophoretic injections of Phaseolus vulgaris leucoagglutinin into layer IV. The neurochemical content of both pre- and postsynaptic profiles was identified by postembedding immunocytochemistry for gamma-amino butyric acid (GABA) and glutamate. Sizes of pre- and postsynaptic elements were quantified by using an image analysis system, BioQuant IV. Our chief finding is that K LGN axons and layer IV axons (indirect input from M and P pathways) exhibit different synaptic relationships to CO blob cells. Specifically, our results show that within the CO blobs: 1) all K cell axons contain glutamate, and the vast majority of layer IV axons contain glutamate with only 5% containing GABA; 2) K axons terminate mainly on dendritic spines of glutamatergic cells, while layer IV axons terminate mainly on dendritic shafts of glutamatergic cells; 3) K axons have larger boutons and contact larger postsynaptic dendrites, which suggests that they synapse closer to the cell body within the CO blobs than do layer IV axons. Taken together, these results suggest that each input pathway to the CO blobs uses a different strategy to contribute to the processing of visual information within these compartments.

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The postnatal development of geniculocortical axon arbors in owl monkeys

Cited by 19 publications

References 68 publications

Neurochemical comparison of synaptic arrangements of parvocellular, magnocellular, and koniocellular geniculate pathways in owl monkey (Aotus trivirgatus) visual cortex

Neurochemical comparison of synaptic arrangements of parvocellular, magnocellular, and koniocellular geniculate pathways in owl monkey (Aotus trivirgatus) visual cortex

Postnatal Development of Binocular Disparity Sensitivity in Neurons of the Primate Visual Cortex

Synaptic and neurochemical characterization of parallel pathways to the cytochrome oxidase blobs of primate visual cortex

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