Neuropeptide Y-Containing Neurons are Situated Predominantly Outside Cytochrome Oxidase Puffs in Macaque Visual Cortex

Kuljiš, Rodrigo O.; Rakić, Paško

doi:10.1017/s0952523800004326

Cited by 32 publications

(18 citation statements)

References 29 publications

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“…2). They had the morphological features of aspiny stellate neurons, which are characteristic of this region in normal adults (13,17). Although NPY-containing neurons were found in the blobs and in the interblob regions of the normal and enucleated animals, even cursory examination revealed that the majority of these neurons were situated in the interblob regions and very few were located in the blobs (Fig.…”

Section: Resultsmentioning

confidence: 93%

Section: Methodsmentioning

confidence: 99%

“…Immunolabeled stellate neurons in the blobs, in interblob regions, and at the interface between them were counted. The total area of layers 11/111 and that occupied by blobs were measured by computerized planimetry (13).…”

Section: Methodsmentioning

confidence: 99%

“…Blobs and interblob regions also differ in the patterns of cortical and subcortical connectivity, which may explain, in part, their distinct physiological properties (6)(7)(8)(9)(10)(11)(12). We reported recently that the density of neuropeptide Y (NPY)-containing neurons in macaque monkey is significantly higher in interblob regions than within blobs, indicating that they also differ in their respective arrays of local circuit neurons (13).…”

Section: Introductionmentioning

confidence: 99%

“…The nearly flat shape of the opercular region allowed precise sectioning parallel to the pial surface at 40-gum intervals. Series of alternate sections were labeled histochemically for CytOx (6-13) or for NPY-like immunoreactivity by the avidin/biotin/peroxidase method (16), as described previously (13,17).Computer-assisted two-dimensional plots of the distribution of NPY-containing neurons were obtained from tangential sections and aligned with camera lucida drawings of the CytOx blobs in adjacent sections. In order to align precisely adjacent regions, we used the perpendicularly perforating blood vessels, which exhibit an identical pattern among sections.…”

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confidence: 99%

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Hypercolumns in primate visual cortex can develop in the absence of cues from photoreceptors.

Kuljiš

Rakić

1990

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

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The visual cortex in primates consists of an array of anatomically and chemically identifiable cellular modules (hypercolumns) with distinct physiological properties. For example, layers II/III in the macaque monkey contain a regular array of cytochrome oxidase-rich blobs. Furthermore, the surrounding cytochrome oxidase-poor interblob regions have a higher density of neuropeptide Y-positive aspiny stellate cells. Neurons in the blobs are thought to mediate predominantly low spatial frequencies and color vision, while those in the interblobs appear to be engaged in pattern vision and high spatial frequency analysis. In this study we examined the role of the retina in the development of hypercolumns. A bilateral retinal ablation was performed in embryos at midgestation, before any photoreceptors had established contacts with other retinal neurons and before layers II/III of the cortex-or their synaptic connection-had been generated. We found that the cortex in operated animals had cytochrome oxidase blobs and that their size and spacing were normal. In addition, neuropeptide Y-containing neurons were preferentially distributed in the interblob region as in control animals. Our findings indicate that some basic aspects of the cyto-and chemoarchitectonic organization of the cerebral cortex, which presumably evolved for the analysis of form and color, can emerge in the absence of cues from the retinal photoreceptors that mediate these attributes of vision.The cerebral neocortex is composed of many distinct cytoarchitectonic areas, each of which is an aggregate of modular compartments with characteristic anatomical, chemical, and physiological properties (1-3). The mechanisms that control the development and differentiation of these compartments are not known, although they may be important for understanding the evolution of the neocortex and the biological basis of human cognition. This modular organization is perhaps best characterized in the macaque monkey primary visual (striate) cortex (4, 5). In layers II/III of this area, the cytochrome oxidase (CytOx)-containing blobs (variably called also puffs, dots, patches, or spots) are distributed in columns of cells whose spatial frequency tuning as well as chromatic and orientation-selective receptive field properties are different from cells situated in columns in the surrounding interblob regions (6-9). Blobs and interblob regions also differ in the patterns of cortical and subcortical connectivity, which may explain, in part, their distinct physiological properties (6-12). We reported recently that the density of neuropeptide Y (NPY)-containing neurons in macaque monkey is significantly higher in interblob regions than within blobs, indicating that they also differ in their respective arrays of local circuit neurons (13).Several of the questions raised by these findings are as follows. To what extent does the development of cytochemical differences between blobs and interblob regions, which may mediate distinct aspects of visual function such as the percepti...

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Section: Resultsmentioning

confidence: 93%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Hypercolumns in primate visual cortex can develop in the absence of cues from photoreceptors.

Kuljiš

Rakić

1990

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

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Differential glutamatergic innervation in cytochrome oxidase-rich and -poor regions of the macaque striate cortex: Quantitative EM analysis of neurons and neuropil

Nie

Wong‐Riley

1996

J. Comp. Neurol.

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One of the hallmarks of the primate striate cortex is the presence of cytochrome oxidase (CO)-rich puffs and CO-poor interpuffs in its supragranular layers. However, the neurochemical basis for their differences in metabolic activity and physiological properties is not well understood. The goals of the present study were to determine whether CO levels in postsynaptic neuronal compartments were correlated with the proportion of excitatory glutamate-immunoreactive (Glu-IR) synapses they received and if Glu-IR terminals and synapses in puffs differed from those in interpuffs. By combining CO histochemistry and postembedding Glu immunocytochemistry on the same ultrathin sections, the simultaneous distribution of the two markers in individual neuronal profiles was quantitatively analyzed. As a comparison, adjacent sections were identically processed for the double labeling of CO and GABA, an inhibitory neurotransmitter. In both puffs and interpuffs, most axon terminals forming asymmetric synapses (84%)--but not symmetric ones, which were GABA-IR--were intensely immunoreactive for Glu. GABA-IR neurons received mainly Glu-IR synapses on their cell bodies, and they had three times as many mitochondria darkly reactive for CO than Glu-rich neurons, which received only GABA-IR axosomatic synapses. In puffs, GABA-IR neurons received a significantly higher ratio of Glu-IR to GABA-IR axosomatic synapses and contained about twice as many darkly CO-reactive mitochondria than those in interpuffs. There were significantly more Glu-IR synapses and a higher ratio of Glu- to GABA-IR synapses in the neuropil of puffs than of interpuffs. Moreover, Glu-IR axon terminals in puffs contained approximately three times more darkly CO-reactive mitochondria than those in interpuffs, suggesting that the former may be synaptically more active. Thus, the present results are consistent with our hypothesis that the levels of oxidative metabolism in postsynaptic neurons and neuropil are positively correlated with the proportion of excitatory synapses they receive. Our findings also suggest that excitatory synaptic activity may be more prominent in puffs than in interpuffs, and that the neurochemical and synaptic differences may constitute one of the bases for physiological and functional diversities between the two regions.

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Effects of aging on numbers and sizes of neurons in histochemically defined subregions of monkey striate cortex

1997

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Background In addition to its horizontal layers, primate striate cortex has a vertical modular organization. Among the vertical modules are histochemically defined areas of high and low cytochrome oxidase labeling in the supragranular layers, referred to, respectively, as blobs and interblobs. Cytochrome c oxidase (CO) blobs and interblobs differ in their inputs from the magnocellular and parvocellular visual pathways, their physiological properties, and many aspects of their neurochemistry. The present study investigated whether aging differentially affects neuron numbers or sizes in the supragranular blobs or interblobs. Methods The right hemisphere from three young adult (5.2–12.4 years) and four old (24.0–26.7 years) rhesus monkeys was used. Tangential sections through the central visual‐field representation were stained for CO and counterstained with cresyl violet. Montages were constructed through cortical layers 2 and 3, and neuron counts and size measurements were made in blob and interblob regions using stereological procedures that yield unbiased estimates. Blob density also was calculated. Results CO blob density was 3.76/mm2 in young adults and 3.95/mm2 in old animals, a difference that was not statistically significant. Neuron soma sizes also did not differ significantly between young adult and old animals or between blob and interblob regions. In addition, neuron density was not significantly different between young adult and old animals. However, independent of age, neuron density was significantly higher in the center of interblobs (394,058 cells/mm3) than in the center of blobs (333,638/mm3). Conclusions Our results and those of previous studies (Vincent et al. 1989. Anat. Rec.223:329–341; Peters and Sethares. 1993. Anat. Rec.236:721–729) suggest that aging has little or no effect on the densities or sizes of the different functional or morphological types of neurons that exist in the different cortical layers or in the different vertical modules marked by CO blobs and interblobs. These findings are consistent with the results of our previous anatomical and physiological studies of the rhesus monkey retina and lateral geniculate nucleus. These results suggest that the retinogeniculostriate pathways are relatively unaffected by aging in the rhesus monkey. Anat. Rec. 247:119–128 © 1997 Wiley‐Liss, Inc.

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Neuropeptide Y-Containing Neurons are Situated Predominantly Outside Cytochrome Oxidase Puffs in Macaque Visual Cortex

Cited by 32 publications

References 29 publications

Hypercolumns in primate visual cortex can develop in the absence of cues from photoreceptors.

Hypercolumns in primate visual cortex can develop in the absence of cues from photoreceptors.

Differential glutamatergic innervation in cytochrome oxidase-rich and -poor regions of the macaque striate cortex: Quantitative EM analysis of neurons and neuropil

Effects of aging on numbers and sizes of neurons in histochemically defined subregions of monkey striate cortex

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