Quantitative light and electron microscopic analysis of cytochrome oxidase‐rich zones in the striate cortex of the squirrel monkey

Cytochrome oxidase activity was examined in the striate cortex (area 17) of squirrel monkeys at both the light and ultrastructural levels. Two prominent bands of reactivity were found in 4A and 4C with intermittent puffs of cytochrome oxidase reactivity in laminae 2 and 3. These puffs, spaced 0.5 mm apart, were in register with intermittent concentrations of activity in laminae 4B, 5, and 6. A thin band of reactivity was observed in lamina 1. The upper portion of 4Cβ was less reactive than 4Cα or the lower portion of 4Cβ. Reactive neurons included stellate cells in all laminae and pyramidal cells in laminae 2 through 4B, 5, and 6. A row of large reactive pyramidal cells was observed in upper lamina 6. More reactive neurons were found in the puffs (laminae 2 and 3) than were observed in interpuff regions, and the reactive neurons were significantly larger than the nonreactive neurons. Reactive neurons contained two to three times as many reactive mitochondria as did the nonreactive neurons and often had indented nuclei. Based on the number of darkly or highly reactive, moderately reactive and lightly reactive mitochondria, puff regions were significantly different from nonpuff regions; there were approximately two times as many darkly reactive mitochondria in puff regions as compared to a similar nonpuff area. The majority of mitochondria (32% in puff; 44% in nonpuff) were found to reside in the dendritic profiles, which also contained the majority of highly reactive mitochondria. In a separate analysis, the total area of highly reactive mitochondria within puff regions was found to be twice the total area of highly reactive mitochondria in a comparable nonpuff region. An analysis of synapses showed that there were more asymmetrical synapses in both puff and nonpuff regions (55% and 54%, respectively) than symmetrical ones (45% in puff and 46% in nonpuff). There was an increase in mitochondrial reactivity in both asymmetrical and symmetrical synapses in the puff areas; however, the increased reactivity within asymmetrical terminals was significantly greater than that within symmetrical ones. Several somatodendritic synapses were observed and they were all of the symmetrical variety. Axospinous contacts were primarily of the asymmetrical type; however, symmetrical axospinous synapses were observed and were typically seen in association with an asymmetrical synapse.

[1]  C. Curcio,et al.  Organization of pulvinar afferents to area 18 in the squirrel monkey: evidence for stripes , 1978, Brain Research.

[2]  A. Peters,et al.  The forms of non‐pyramidal neurons in the visual cortex of the rat , 1978, The Journal of comparative neurology.

[3]  M. Wong-Riley.  Reciprocal connections between striate and prestriate cortex in squirrel monkey as demonstrated by combined peroxidase histochemistry and autoradiography , 1978, Brain Research.

[4]  J. Tigges,et al.  Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in squirrel monkey (Saimiri) , 1981, The Journal of comparative neurology.

[5]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[6]  K. Krab,et al.  Cytochrome oxidase : a synthesis , 1981 .

[7]  K. Uchizono.  Characteristics of Excitatory and Inhibitory Synapses in the Central Nervous System of the Cat , 1965, Nature.

[8]  M. Wong-Riley,et al.  The effect of impulse blockage on cytochrome oxidase activity in the cat visual system , 1983, Brain Research.

[9]  A. Cowey.  PROJECTION OF THE RETINA ON TO STRIATE AND PRESTRIATE CORTEX IN THE SQUIRREL MONKEY, SAIMIRI SCIUREUS. , 1964, Journal of neurophysiology.

[10]  S. Palay,et al.  Meynert cells in the primate visual cortex , 1974, Journal of neurocytology.

[11]  R. Coggeshall,et al.  Branching of sensory axons in the dorsal root and evidence for the absence of dorsal root efferent fibers , 1979, The Journal of comparative neurology.

[12]  C. Ribak,et al.  Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase , 1978, Journal of neurocytology.

[13]  J R Wolff,et al.  Axosomatic synapses in the visual cortex of adult rat. A comparison between GABA-accumulating and other neurons , 1982, Journal of neurocytology.

[14]  A. Lehninger.  Biochemistry: The Molecular Basis of Cell Structure and Function , 1970 .

[15]  D. Fitzpatrick,et al.  The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus) , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  V. Casagrande,et al.  The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons , 1978, Brain Research.

[17]  R. Friede,et al.  Topographic Brain Chemistry , 1966 .

[18]  M. Wong-Riley.  Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[19]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[20]  M. Colonnier.  Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[21]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

[22]  J. Tigges,et al.  Complementary laminar terminations of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey , 1977, The Journal of comparative neurology.

[23]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

[24]  Alan Peters,et al.  Smooth and sparsely‐spined stellate cells in the visual cortex of the rat: A study using a combined golgi‐electron microscope technique , 1978, The Journal of comparative neurology.

[25]  L. Garey.  A light and electron microscopic study of the visual cortex of the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[26]  A. Cowey,et al.  Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey , 1981, Nature.

[27]  J. Kaas,et al.  The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. , 1974, Brain research.

[28]  G. Henry,et al.  Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey , 1979, The Journal of comparative neurology.

[29]  J. Lund,et al.  Anatomical organization of primate visual cortex area VII , 1981, The Journal of comparative neurology.

[30]  J. K. Harting,et al.  Ascending pathways from the monkey superior colliculus: An autoradiographic analysis , 1980, The Journal of comparative neurology.

[31]  J. Tigges,et al.  Efferent cortico‐cortical fiber connections of area 18 in the squirrel monkey (Saimiri) , 1974, The Journal of comparative neurology.

[32]  A. Peters,et al.  Chandelier cells in rat visual cortex , 1982, The Journal of comparative neurology.

[33]  S. Zeki.  Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[34]  J. Szentágothai.  The Ferrier Lecture, 1977 The neuron network of the cerebral cortex: a functional interpretation , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[35]  Michael M. Merzenich,et al.  Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity , 1978, Brain Research.

[36]  L. Iversen,et al.  Selective accumulation of [3H]GABA by stellate cells in rat cerebellar cortexin vivo , 1972 .

[37]  J. Lund.  Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[38]  E. Jones,et al.  Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  D. B. Bender,et al.  Receptive-field properties of neurons in the macaque inferior pulvinar. , 1982, Journal of neurophysiology.

[40]  J. Kaas,et al.  Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates , 1978, The Journal of comparative neurology.

[41]  D. Hubel,et al.  Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[42]  G. Poggio,et al.  Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. , 1977, Journal of neurophysiology.

[43]  M. Wong-Riley,et al.  Maintenance of Neuronal Activity by Electrical Stimulation of Unilaterally Deafened Cats Demonstrable with Cytochrome Oxidase Technique , 1981, The Annals of otology, rhinology & laryngology. Supplement.

[44]  M. Ogren,et al.  The neurological organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in old world and new world primates , 1978, The Journal of comparative neurology.

[45]  T. Tömböl,et al.  An electron microscopic study of the neurons of the visual cortex , 1974, Journal of neurocytology.

[46]  J. Baizer,et al.  Visual responses of area 18 neurons in awake, behaving monkey. , 1977, Journal of neurophysiology.

[47]  F. Ebner,et al.  A quantitative study of synaptic patterns in turtle visual cortex , 1978, The Journal of comparative neurology.

[48]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[49]  R. Whittam,et al.  The metabolic response of brain slices to agents affecting the sodium pump , 1967, The Journal of physiology.

[50]  T. Powell,et al.  The number and distribution of Meynert cells in area 17 of the macaque monkey , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[51]  P. Somogyi,et al.  The study of golgi stained cells and of experimental degeneration under the electron microscope: A direct method for the identification in the visual cortex of three successive links in a neuron chain , 1978, Neuroscience.

[52]  M. Wong-Riley.  Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys , 1979, Brain Research.

[53]  le Gros Clark We,et al.  The cells of Meynert in the visual cortex of the monkey. , 1942 .

[54]  A. Hendrickson,et al.  Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex , 1981, Nature.

[55]  A. Hendrickson,et al.  Pathways between striate cortex and subcortical regions in Macaca mulatta and Saimiri sciureus: Evidence for a reciprocal pulvinar connection , 1976, Experimental Neurology.

[56]  L. Benevento,et al.  The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (macaca mulatta): An autoradiographic study , 1976, Brain Research.

[57]  B. Cragg.  The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. , 1969, Vision research.

[58]  M. Wong-Riley,et al.  Histochemical localization of cytochrome oxidase in the hippocampus: Correlation with specific neuronal types and afferent pathways , 1982, Neuroscience.

[59]  J. Tigges,et al.  Species difference between Old World and New World monkeys in the organization of the striate-prestriate association. , 1972, Brain research.

[60]  A. Hendrickson,et al.  The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey , 1977, Brain Research.

[61]  W. B. Spatz.  An efferent connection of the solitary cells of Meynert. A study with horseradish peroxidase in the marmoset Callithrix , 1975, Brain Research.

[62]  Luis Martinez-Milla´n,et al.  Cortico-cortical projections from striate cortex of the squirrel monkey (Saimiri sciureus). A radioautographic study , 1975, Brain Research.

[63]  J. E. Vaughn,et al.  The GABA Neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry , 1979, The Journal of comparative neurology.

[64]  Peter Grigg,et al.  Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal , 1974 .

[65]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[66]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[67]  J. Tigges,et al.  Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri) , 1970, The Journal of comparative neurology.

[68]  M. Wong-Riley,et al.  Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[69]  The histochemical localization of cytochrome oxidase in the dentate gyrus of the rat hippocampus , 1981, Brain Research.

[70]  J. Szentágothai.  The ‘module-concept’ in cerebral cortex architecture , 1975, Brain Research.

[71]  O. H. Lowry,et al.  The quantitative histochemistry of brain. III. Ammon's horn. , 1954, The Journal of biological chemistry.

[72]  M. Silverman,et al.  Functional organization of the second cortical visual area in primates. , 1983, Science.

[73]  H. Hess,et al.  Intralaminar distribution of cytochrome oxidase and DPN in rat cerebral cortex. , 1956, Journal of neurophysiology.

[74]  Margaret T. T. Wong-Riley,et al.  Connections between the pulvinar nucleus and the prestriate cortex in the squirrel monkey as revealed by peroxidase histochemistry and autoradiography , 1977, Brain Research.

[75]  J. Trojanowski,et al.  Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey , 1976, The Journal of comparative neurology.

[76]  J. Kaas,et al.  Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[77]  M. Wong-Riley.  Endogenous peroxidatic activity in brain stem neurons as demonstrated by their staining with diaminobenzidine in normal squirrel monkeys , 1976, Brain Research.

[78]  Thomas T. Norton,et al.  Organization of ocular dominance in tree shrew striate cortex , 1977, Brain Research.

[79]  J. Lund,et al.  Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the Macaque monkey , 1975 .

[80]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[81]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.