Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T10:32:52.143Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Rodrigo O. Kuljis  and
Pasko Rakic
Rodrigo O. Kuljis
Affiliation:
Section of Neuroanatomy, Yale University School of Medicine, New Haven
Pasko Rakic
Affiliation:
Section of Neuroanatomy, Yale University School of Medicine, New Haven
Get access Rights & Permissions [Opens in a new window]

Abstract

Layers II/III of the primary visual cortex contain a regular pattern of histochemically detectable cytochrome oxidase (CO)-rich “puffs,” which differ from the interpuff regions in their thalamo-cortical and cortico-cortical connectivity, receptive-field properties, and the density of inhibitory GABA-containing synaptic terminals. We used an immunocytochemical method, in combination with cytochrome oxidase histochemistry, to analyze the spatial relationship between neurons that contain neuropeptide Y (NPY) and the CO puffs. Of a total of 606 neurons, only 2.6% of the NPY-containing cells are located in the puffs, whereas the rest are situated in the interpuffs, or at the interface between puffs and interpuffs. The number of NPY-containing neurons in the puffs is substantially less than that expected in an equal volume of the interpuffs (X2 = 13.86; df = 1; P < 0.001).

These observations indicate that columns containing the puffs may differ also from those in the interpuff regions in that they contain a unique array of chemically and morphologically distinct local circuit neurons.

Keywords

Neuropeptide YCytochrome oxidaseStriate cortexMacaque monkeyLocal circuit neurons
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 1 , January 1989 , pp. 57 - 62
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Berod, A., Hartman, B.K., & Pujol, J.F. (1981). Importance of fixation in immunocytochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. Journal of Histochemistry and Cytochemistry 29, 844–850.CrossRefGoogle ScholarPubMed
Carrol, E.W. & Wong-Riley, M.T.T. (1984). Quantitative and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 1–17.CrossRefGoogle Scholar
Carrol, E.W. & Wong-Riley, M.T.T. (1985). Correlation between cytochrome oxidase and the uptake and laminar distribution of tritiated aspartate, glutamate, γ-aminobutyrate and glycine in the striate cortex of the squirrel monkey. Neuroscience 15, 959–976.CrossRefGoogle Scholar
Creutzfeldt, O.D. (1977). Generality of the functional structure of the neocortex. Naturwissenschaften 64, 507–517.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S., Schmechel, D.E., & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P.S. & Schwartz, M.S. (1982). Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Science 216, 755–757.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P.S. (1988). Topography of cognition: parallel distributed networks in primate association cortex. Annual Reviews of Neuroscience 11, 137–156.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Hunt, S.P., & Wu, J.-Y. (1981). Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605–607.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G. & Emson, P.C. (1984 a). Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. Journal of Neuroscience 4, 2497–2517.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., DeFelipe, J., Schmechel, D., Brandon, C. & Emson, P.C. (1984 b). Neuropeptide-containing neurons in the cerebral cortex are also GABAergic. Proceedings of the National Academy of Sciences of the U.S.A. 81, 6526–6530.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle ScholarPubMed
Horton, J.C. (1984). Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society of London, B 304, 199–253.Google ScholarPubMed
Hsu, S.-M., Raine, L., & Fanger, F. (1981). Use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques. Journal of Histochemistry and Cytochemistry 29, 577–580.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1977). Functional architecture of macaque visual cortex. Philosophical Transactions of the Royal Society of London, B 198, 1–59.Google Scholar
Hubel, D.H. & Livingstone, M.S. (1985). Complex-unoriented cells in a subregion of primate area 18. Nature 315, 325–327.CrossRefGoogle Scholar
Kuljis, R.O. & Rakic, P. (1988 a). Multiple types of neuropeptide Y-containing neurons in primate neocortex. Journal of Comparative Neurology (in press).Google Scholar
Kuljis, R.O. & Rakic, P. (1988 b). Distribution of neuropeptide Y-containing perikarya and axons in various neocortical areas of the macaque monkey. Journal of Comparative Neurology (in press).Google Scholar
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6098–6101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 a). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 b). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Mountcastle, V.B. (1957). Modality and topographic properties of single neurons of cat's sensory cortex. Journal of Neurophysiology 20, 408–434.CrossRefGoogle ScholarPubMed
Mountcastle, V.B. (1978). An organizing principle for cerebral function: the unit module and the distributed system. In The Mindful Brain, ed. Edelman, G.M. & Mountcastle, V.B., pp. 7–50. Cambridge, MA: MIT Press.Google Scholar
Schwartz, M.L. & Goldman-Rakic, P.S. (1988). Periodicity of GABA-containing cells in primate prefrontal cortex. Journal of Neuroscience 8, 1962–1970.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–325.CrossRefGoogle ScholarPubMed
Somogyi, P. & Takagi, H. (1982). A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neuroscience 7, 1779–1793.CrossRefGoogle ScholarPubMed
Somogyi, P., Hodgson, A.J., Smith, A.D., Nunci, M.G., Gorio, A. & Wu, J.-Y. (1984). Different populations of GABAergic neurons in the visual cortex and hippocampus of cat containing somatostatin- or cholecystokinin-immunoreactive material. Journal of Neuroscience 4, 2590–2603.CrossRefGoogle ScholarPubMed
Somogyi, P. (1987). Synaptic organization and transmitters of transcortical circuits. In Cerebral Cortex as a Unified Structure, ed. Goldman-Rakic, P., pp. 37–53. Washington, D.C.: Society for Neuroscience.Google Scholar
Sternberger, L. (1986). Immunocytochemistry. New York: Alan R. Liss.Google Scholar
Szenthágothai, J. (1975). The “module-concept” in cerebral cortex architecture. Brain Research 95, 475–496.CrossRefGoogle Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocularly sutured or enucleated kittens demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Carrol, E.W. (1984 a). Quantitative and electron microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 18–37.CrossRefGoogle Scholar
Wong-Riley, M.T.T. & Carroll, E.W. (1984 b). Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262–264.CrossRefGoogle ScholarPubMed