Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Original Paper

Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans

II. Stereologic Analysis of Chemoarchitecture

Sherwood C.C.a-d · Holloway R.L.a,c · Erwin J.M.d · Hof P.R.b-d

Author affiliations

aDepartment of Anthropology, Columbia University, bKastor Neurobiology of Aging Laboratory and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, cNew York Consortium in Evolutionary Primatology, New York, N.Y., and dFoundation for Comparative and Conservation Biology, Rockville, Md., USA

Related Articles for ""

Brain Behav Evol 2004;63:82–106

Do you have an account?

Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 9.00 *
EUR 8.00 *
USD 9.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.
Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00


Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: July 01, 2003
Accepted: August 27, 2003
Published online: February 06, 2004
Issue release date: February 2004

Number of Print Pages: 25
Number of Figures: 13
Number of Tables: 4

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

Abstract

This study presents a comparative stereologic investigation of neurofilament protein- and calcium-binding protein-immunoreactive neurons within the region of orofacial representation of primary motor cortex (Brodmann’s area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). Results showed that the density of interneurons involved in vertical interlaminar processing (i.e., calbindin- and calretinin-immunoreactive neurons) as well pyramidal neurons that supply heavily-myelinated projections (i.e., neurofilament protein-immunoreactive neurons) are correlated with overall neuronal density, whereas interneurons making transcolumnar connections (i.e., parvalbumin-immunoreactive neurons) do not exhibit such a relationship. These results suggest that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry. For example, cortical columns across catarrhine species appear to involve a similar conserved network of intracolumnar inhibitory interconnections, as represented by the distribution of calbindin- and calretinin-immunoreactive neurons. The subpopulation of horizontally-oriented wide-arbor interneurons, on the other hand, increases in density relative to other interneuron subpopulations in large brains. Due to these scaling trends, the region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined. These modifications might contribute to the voluntary dexterous control of orofacial muscles in great ape and human communication.

© 2004 S. Karger AG, Basel


References

  1. Akil M, Lewis DA (1992a) Differential distribution of parvalbumin-immunoreactive pericellular clusters of terminal boutons in developing and adult monkey neocortex. Exp Neurol 115:239–249.
  2. Akil M, Lewis DA (1992b) Postnatal development of parvalbumin immunoreactivity in axon terminals of basket and chandelier neurons in monkey neocortex. Prog Neuropsychopharmacol Biol Psych 16:329–337.
  3. Alcantara S, Ferrer I (1994) Postnatal development of parvalbumin immunoreactivity in the cerebral cortex of the cat. J Comp Neurol 348:133–149.
  4. Alcantara S, Ferrer I, Soriano E (1993) Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol (Berl) 188:63–73.
  5. Alipour M, Chen Y, Jürgens U (2002) Anterograde projections of the motorcortical tongue area in the saddle-back tamarin (Saguinus fuscicollis). Brain Behav Evol 60:101–116.
  6. Andressen C, Blümcke I, Celio MR (1993) Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res 271:181–208.
  7. Baimbridge KG, Miller JJ (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223–229.
  8. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308.
  9. Baleydier C, Achache P, Froment JC (1997) Neurofilament architecture of superior and mesial premotor cortex in the human brain. NeuroReport 8:1691–1696.
  10. Belichenko PV, Vogt Weisenhorn DM, Myklossy J, Celio MR (1995) Calretinin-positive Cajal-Retzius cells persist in the adult human neocortex. NeuroReport 6:1869–1874.
  11. Blümcke I, Hof PR, Morrison JH, Celio MR (1990) Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans. J Comp Neurol 301:417–432.
  12. Blümcke I, Hof PR, Morrison JH, Celio MR (1991) Parvalbumin in the monkey striate cortex: A quantitative immunoelectron-microscopy study. Brain Res 554:237–243.
  13. Bush EC, Allman JM (2003) The scaling of white matter to gray matter in cerebellum and neocortex. Brain Behav Evol 61:1–5.
  14. Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205.
  15. Campbell MJ, Hof PR, Morrison JH (1991) A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein. Brain Res 539:133–136.
  16. Cao QL, Yan XX, Luo XG, Garey LJ (1996) Prenatal development of parvalbumin immunoreactivity in the human striate cortex. Cereb Cortex 6:620–630.
  17. Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402.
  18. Celio MR (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995–997.
  19. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475.
  20. Chadwick-Jones J (1998) Developing a Social Psychology of Monkeys and Apes. East Sussex: Psychology Press.
  21. Chaudhuri A, Zangenehpour S, Matsubara JA, Cynader MS (1996) Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Res 709:17–26.
  22. Colombo JA, Schleicher A, Zilles K (1999) Patterned distribution of immunoreactive astroglial processes in the striate (V1) cortex of New World monkeys. Glia 25:85–92.
  23. Colombo JA, Fuchs E, Hartig W, Marotte LR, Puissant V (2000) ‘Rodent-like’ and ‘primate-like’ types of astroglial architecture in the adult cerebral cortex of mammals: A comparative study. Anat Embryol (Berl) 201:111–120.
  24. Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: Distribution and morphology. J Comp Neurol 341:95–116.
  25. Cusick CG, Seltzer B, Cola M, Griggs E (1995) Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex. J Comp Neurol 360:513–535.
  26. De Lima AD, Voigt T, Morrison JH (1990) Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. J Comp Neurol 296:159–272.
  27. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28k, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1–19.
  28. DeFelipe J, Farinas I (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39:563–607.
  29. DeFelipe J, Hendry SH, Jones EG (1986) A correlative electron microscopic study of basket cells and large GABAergic neurons in the monkey sensory-motor cortex. Neuroscience 17:991–1009.
  30. DeFelipe J, Hendry SH, Jones EG (1989a) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res 503:49–54.
  31. DeFelipe J, Hendry SH, Jones EG (1989b) Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc Natl Acad Sci U S A 86:2093–2097.
  32. DeFelipe J, Hendry SH, Jones EG, Schmechel D (1985) Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J Comp Neurol 231:364–384.
  33. DeFelipe J, Jones EG (1985) Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. J Neurosci 5:3246–3260.
  34. del Rio MR, DeFelipe J (1994) A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temporal neocortex. J Comp Neurol 342:389–408.
  35. del Rio MR, DeFelipe J (1996) Colocalization of calbindin D-28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex. J Comp Neurol 369:472–482.
  36. del Rio MR, DeFelipe J (1997) Colocalization of parvalbumin and calbindin D-28k in neurons including chandelier cells of the human temporal neocortex. J Chem Neuroanat 12:165–173.
  37. Demeulemeester H, Arckens L, Vandesande F, Orban GA, Heizmann CW, Pochet R (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp Brain Res 84:538–544.
  38. Demeulmeester H, Vandesande F, Orba GA, Brandon C, Vanderhaegen JJ (1988) Heterogeneity of GABAergic cells in cat visual cortex. J Neurosci 8:988–1000.
  39. Donoghue JP, Leibovic S, Sanes JN (1992) Organization of the forelimb area in squirrel monkey motor cortex: Representation of digit, wrist, and elbow muscles. Exp Brain Res 89:1–19.
  40. Fairén A, DeFelipe J, Regidor J (1984) Nonpyramidal neurons: general account. In: Cerebral Cortex 1, Cellular Components of the Cerebral Cortex (Peters A, Jones EG, eds), pp 210–253. New York: Plenum Press.
  41. Fay RA, Norgren R (1997) Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus. III. Lingual muscle motor systems. Brain Res Rev 25:291–311.
  42. Ferrer I, Zujar MJ, Admella C, Alcantara S (1992) Parvalbumin and calbindin immunoreactivity in the cerebral cortex of the hedgehog (Erinaceus europaeus). J Anat 180:165–174.
    External Resources
  43. Fonseca M, del Rio JA, Martinez A, Gomez S, Soriano E (1995) Development of calretinin immunoreactivity in the neocortex of the rat. J Comp Neurol 361:177–192.
  44. Fonseca M, Soriano E (1995) Calretinin-immunoreactive neurons in the normal human temporal cortex and in Alzheimer’s disease. Brain Res 691:83–91.
  45. Fonseca M, Soriano E, Ferrer I, Martinez A, Tunon T (1993) Chandelier cell axons identified by parvalbumin-immunoreactivity in the normal human temporal cortex and in Alzheimer’s disease. Neuroscience 55:1107–1116.
  46. Freund TF, Martin KA, Smith AD, Somogyi P (1983) Glutamate decarboxylase-immunoreactive terminals of Golgi-impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat’s visual cortex. J Comp Neurol 221:263–278.
  47. Freund TF, Buzsaki G, Leon A, Baimbridge KG, Somogyi P (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp Brain Res 83:55–66.
  48. Gabbott PL, Bacon SJ (1996a) Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey. II. Quantitative areal and laminar distributions. J Comp Neurol 364:609–636.
  49. Gabbott PL, Bacon SJ (1996b) Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey. I. Cell morphology and morphometrics. J Comp Neurol 364:567–608.
  50. Gabbott PL, Jays PR, Bacon SJ (1997a) Calretinin neurons in human medial prefrontal cortex (areas 24a,b,c, 32’, and 25). J Comp Neurol 381:389–410.
  51. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ (1997b) Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution. J Comp Neurol 377:465–499.
  52. Gabernet L, Meskenaite V, Hepp-Reymond MC (1999) Parcellation of the lateral premotor cortex of the macaque monkey based on staining with the neurofilament antibody SMI-32. Exp Brain Res 128:188.
  53. Gattass R, Adams MM, Hof PR, Ungerleider LG (1996) Parcellation of visual cortical areas in the chimpanzee using neurofilament and calcium-binding proteins. Soc Neurosci Abst 22:1059.
  54. Geyer S, Zilles K, Luppino G, Matelli M (2000) Neurofilament protein distribution in the macaque monkey dorsolateral premotor cortex. Eur J Neurosci 12:1554–1566.
  55. Glezer, II, Hof PR, Leranth C, Morgane PJ (1993) Calcium-binding protein-containing neuronal populations in mammalian visual cortex: A comparative study in whales, insectivores, bats, rodents, and primates. Cereb Cortex 3:249–272.
  56. Glezer, II, Hof PR, Morgane PJ (1992) Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Res 595:181–188.
  57. Glezer, II, Hof PR, Morgane PJ (1998) Comparative analysis of calcium-binding protein-immunoreactive neuronal populations in the auditory and visual systems of the bottlenose dolphin (Tursiops truncatus) and the macaque monkey (Macaca fascicularis). J Chem Neuroanat 15:203–237.
  58. Hayes TL, Lewis DA (1992) Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cereb Cortex 2:56–67.
  59. Hayes TL, Lewis DA (1995) Anatomical specializations of the anterior motor speech area: Hemispheric differences in magnopyramidal neurons. Brain Lang 49:289–308.
  60. Heffner R, Masterton B (1975) Variation in form of the pyramidal tract and its relationship to digital dexterity. Brain Behav Evol 12:161–200.
  61. Heffner RS, Masterton RB (1983) The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav Evol 23:165–183.
  62. Heimer L, Robards M (1981) Neuroanatomical Tract-tracing Methods. New York: Plenum Press.
  63. Hendry SH, Jones EG (1991) GABA neuronal subpopulations in cat primary auditory cortex: Co-localization with calcium binding proteins. Brain Res 543:45–55.
  64. Hendry SHC, Schwark HD, Jones EG, Yan J (1987) Number and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503–1519.
  65. Hendry SHC, Jones EG, Emson PC, Lowson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472.
  66. Hiscock JJ, Mackenzie L, Willoughby JO (1998) Laminar distribution of Fos/calcium-binding protein and Fos/neurofilament protein-labeled neurons in rat motor and sensory cortex after picrotoxin-induced seizures. Exp Neurol 149:373–383.
  67. Hof PR, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease. II. Primary and secondary visual cortex. J Comp Neurol 301:55–64.
  68. Hof PR, Morrison JH (1991) Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer’s disease. Exp Neurol 111:293–301.
  69. Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. J Comp Neurol 352:161–186.
  70. Hof PR, Nimchinsky EA (1992) Regional distribution of neurofilament and calcium-binding proteins in the cingulate cortex of the macaque monkey. Cereb Cortex 2:456–467.
  71. Hof PR, Bogaert YE, Rosenthal RE, Fiskum G (1996a) Distribution of neuronal populations containing neurofilament protein and calcium-binding proteins in the canine neocortex: Regional analysis and cell typology. J Chem Neuroanat 11:81–98.
  72. Hof PR, Cox K, Young WG, Celio MR, Rogers J, Morrison JH (1991) Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer’s disease. J Neuropathol Exp Neurol 50:451–462.
  73. Hof PR, Glezer II, Archin N, Janssen WG, Morgane PJ, Morrison JH (1992) The primary auditory cortex in cetacean and human brain: A comparative analysis of neurofilament protein-containing pyramidal neurons. Neurosci Lett 146:91–95.
  74. Hof PR, Glezer II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. J Chem Neuroanat 16:77–116.
    External Resources
  75. Hof PR, Glezer II, Nimchinsky EA, Erwin JM (2000) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: Evidence from primates, cetaceans, and artiodactyls. Brain Behav Evol 55:300–310.
  76. Hof PR, Mufson EJ, Morrison JH (1995b) Human orbitofrontal cortex: Cytoarchitecture and quantitative immunohistochemical parcellation. J Comp Neurol 359:48–68.
  77. Hof PR, Nimchinsky EA, Morrison JH (1995a) Neurochemical phenotype of corticocortical connections in the macaque monkey: Quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. J Comp Neurol 362:109–133.
  78. Hof PR, Nimchinsky EA, Perl DP, Erwin JM (2001) An unusual population of pyramidal neurons in the anterior cingulate cortex of hominids contains the calcium-binding protein calretinin. Neurosci Lett 307:139–142.
  79. Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH (1996b) Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112–127.
  80. Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL (1987) Neurofilament gene expression: A major determinant of axonal caliber. Proc Natl Acad Sci USA 84:3472–3476.
  81. Howard CV, Reed MG (1998) Unbiased Stereology – Three-Dimensional Measurement in Microscopy. New York: Springer-Verlag.
  82. Huber E (1931) Evolution of Facial Musculature and Facial Expression. Baltimore, MD: Johns Hopkins University Press.
  83. Huntley GW, Jones EG (1990) Cajal-Retzius neurons in developing monkey neocortex show immunoreactivity for calcium binding proteins. J Neurocytol 19:200–212.
  84. Huntley GW, Jones EG (1991) Relationship of intrinsic connections of forelimb movement representations in monkey motor cortex: A correlative anatomical and physiological study. J Neurophysiol 66:390–413.
  85. Ichikawa M, Arissian K, Asanuma H (1985) Distribution of corticocortical and thalamocortical synapses on identified motor cortical neurons in the cat: Golgi, electron microscopic and degeneration study. Brain Res 345:87–101.
  86. Iwatsubo T, Kuzuhara S, Kanemitsu A, Shimada H, Toyokura Y (1990) Corticofugal projections to the motor nuclei of the brainstem and spinal cord in humans. Neurology 40:309–312.
  87. Jacobowitz DM, Winsky L (1991) Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304:198–218.
  88. Jande SS, Maler L, Lawson DEM (1981) Immunohistochemical mapping of vitamin D-dependent calcium-binding protein in brain. Nature 2941:765–767.
  89. Jenny AB, Saper CB (1987) Organization of the facial nucleus and corticofacial projection in the monkey: A reconsideration of the upper motor neuron facial palsy. Neurology 37:930–939.
  90. Jones EG, Powell TP (1968) The ipsilateral cortical connexions of the somatic sensory areas in the cat. Brain Res 9:71–94.
  91. Jones EG, Powell TP (1969) Synapses on the axon hillocks and initial segments of pyramidal cell axons in the cerebral cortex. J Cell Sci 5:495–507.
  92. Jones EG, Coulter JD, Hendry SH (1978) Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291–347.
  93. Juliano SL, Friedman DP, Eslin DE (1990) Corticocortical connections predict patches of stimulus-evoked metabolic activity in monkey somatosensory cortex. J Comp Neurol 298:23–39.
  94. Jürgens U, Alipour M (2002) A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neurosci Lett 328:245–248.
  95. Kaneko T, Caria MA, Asanuma H (1994) Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory input and motor output neurons of the cortex. J Comp Neurol 345:161–171.
  96. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387–396.
  97. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476–486.
  98. Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res 416:369–374.
  99. Kirkcaldie MT, Dickson TC, King CE, Grasby D, Riederer BM, Vickers JC (2002) Neurofilament triplet proteins are restricted to a subset of neurons in the rat neocortex. J Chem Neuroanat 24:163–171.
  100. Kisvarday ZF, Beaulieu C, Eysel UT (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition. J Comp Neurol 327:398–415.
  101. Kobayashi K, Emson PC, Mountjoy CQ, Thornton SN, Lawson DE, Mann DM (1990) Cerebral cortical calbindin D28K and parvalbumin neurones in Down’s syndrome. Neurosci Lett 113:17–22.
  102. Kosaka T, Heizmann CW, Tateishi K, Hamaoka Y, Hama K (1987) An aspect of the organizational principle of the gamma-aminobutyric acidergic system in the cerebral cortex. Brain Res 409:403–408.
  103. Künzle H (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in Macaca fascicularis. Brain Behav Evol 15:185–234.
  104. Kuypers HGJM (1958a) Corticobulbar connections to the pons and lower brainstem in man. Brain 81:364–388.
  105. Kuypers HGJM (1958b) Some projections from the peri-central cortex to the pons and lower brainstem in monkey and chimpanzee. J Comp Neurol 110:221–251.
  106. Leichnetz GR (1986) Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8. J Comp Neurol 254:460–492.
  107. Leuba G, Saini K (1997) Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures. J Chem Neuroanat 13:41–52.
  108. Lewis DA, Lund JS (1990) Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin-releasing factor- and parvalbumin-immunoreactive populations. J Comp Neurol 293:599–615.
  109. Lund JS (1987) Local circuit neurons of macaque monkey striate cortex. I. Neurons of laminae 4C and 5A. J Comp Neurol 257:60–92.
  110. Lund JS (1990) Excitatory and inhibitory circuiting and laminar mapping strategies in the primary visual cortex of the monkey. In: Signal and Sense: Local and Global Order in Perceptual Maps (Edelman GM, Gall WE, Cowan WM, eds), pp 51–82. New York: Wiley-Liss.
  111. Lund JS, Lewis DA (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282–312.
  112. Lund JS, Hawken MJ, Parker AJ (1988) Local circuit neurons of macaque monkey striate cortex. II. Neurons of laminae 5B and 6. J Comp Neurol 276:1–29.
  113. Lund JS, Yoshioka T, Levitt JB (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb Cortex 3:148–162.
  114. Lund JS, Yoshioka T, Levitt JB (1994) Substrates for interlaminar connections in area V1 of macaque cerebral cortex. In: Cerebral Cortex. Vol. 10. Primary Visual Cortex in Primates (Peters A, Rockland KS, eds), pp 37–60. New York: Plenum Press.
  115. Martin R, Gutierrez A, Penafiel A, Marin-Padilla M, de la Calle A (1999) Persistence of Cajal-Retzius cells in the adult human cerebral cortex. An immunohistochemical study. Histol Histopathol 14:487–490.
  116. Matelli M, Luppino G, Fogassi L, Rizzolatti G (1989) Thalamic input to inferior area 6 and area 4 in the macaque monkey. J Comp Neurol 280:468–488.
  117. Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113–132.
  118. Mesulam M, Geula C (1991) Differential distribution of a neurofilament protein epitope in acetylcholinesterase-rich neurons of human cerebral neocortex. Brain Res 544:169–173.
  119. Moon JS, Kim JJ, Chang IY, Chung YY, Jun JY, You HJ, Yoon SP (2002) Postnatal development of parvalbumin and calbindin D-28k immunoreactivities in the canine anterior cingulate cortex: Transient expression in layer V pyramidal cells. Int J Dev Neurosci 20:511.
  120. Morecraft RJ, Louie JL, Herrick JL, Stilwell-Morecraft KS (2001) Cortical innervation of the facial nucleus in the non-human primate: A new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. Brain 124:176–208.
    External Resources
  121. Morrison JH, Hof PR, Huntley GW (1998) Neurochemical organization of the primate visual cortex. In: Handbook of Chemical Neuroanatomy (Bloom FE, Björklund A, Hökfelt T, eds), pp 299–430. Amsterdam: Elsevier.
  122. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722.
    External Resources
  123. Mountcastle VB (1998) Perceptual Neuroscience: The Cerebral Cortex. Cambridge, MA: Harvard University Press.
  124. Mouton PR (2002) Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Baltimore and London: The Johns Hopkins University Press.
  125. Nimchinsky EA, Hof PR, Young WG, Morrison JH (1996) Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey. J Comp Neurol 374:136–160.
  126. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1997) Neurofilament and calcium-binding proteins in the human cingulate cortex. J Comp Neurol 384:597–620.
  127. Nixon RA, Sihag RK (1991) Neurofilament phosphorylation: A new look at regulation and function. Trends Neurosci 14:501–506.
  128. Pandya DN, Vignolo LA (1971) Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. Brain Res 26:217–233.
  129. Penfield W, Rasmussen T (1950) The Cerebral Cortex of Man: A Clinical Study of Localization of Function. New York: Macmillan.
  130. Peters A, Harriman KM (1990) Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. I. Morphometric analysis. J Neurocytol 19:154–174.
  131. Phillips CG (1975) Laying the ghost of ‘muscles versus movements’. Can J Neurol Sci 2:209–218.
  132. Pijak DS, Hall GF, Tenicki PJ, Boulos AS, Lurie DI, Selzer ME (1996) Neurofilament spacing, phosphorylation, and axon diameter in regenerating and uninjured lamprey axons. J Comp Neurol 368:569–581.
  133. Porter LL, Sakamoto K (1988) Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat. J Comp Neurol 271:387–396.
  134. Preuss TM, Coleman GQ (2002) Human-specific organization of primary visual cortex: Alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb Cortex 12:671–691.
  135. Preuss TM, Kaas JH (1996) Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates. Brain Res 712:353–357.
    External Resources
  136. Preuss TM, Qi H, Kaas JH (1999) Distinctive compartmental organization of human primary visual cortex. Proc Natl Acad Sci USA 96:11601–11606.
  137. Preuss TM, Stepniewska I, Jain N, Kaas JH (1997) Multiple divisions of macaque precentral motor cortex identified with neurofilament antibody SMI-32. Brain Res 767:148–153.
  138. Qi H, Jain N, Preuss TM, Kaas JH (1999) Inverted pyramidal neurons in chimpanzee sensorimotor cortex are revealed by immunostaining with monoclonal antibody SMI-32. Somatosens Mot Res 16:49–56.
  139. Ren JQ, Aika Y, Heizmann CW, Kosaka T (1992) Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp Brain Res 92:1–14.
  140. Résibois A, Rogers JH (1992) Calretinin in rat brain: An immunohistochemical study. Neuroscience 46:101–134.
  141. Rivara C-B, Sherwood CC, Bouras C, Hof PR (2003) Stereologic characterization and spatial distribution patterns of Betz cells in human primary motor cortex. Anat Rec 270A:137–151.
    External Resources
  142. Rogers JH (1987) Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343–1353.
  143. Ruge G (1887) Untersuchungen über die Gesichtsmuskulatur der Primaten. Leipzig: Engelmann.
  144. Schieber MH (2001) Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 86:2125–2143.
  145. Schierle GS, Gander JC, D’Orlando C, Celio MR, Vogt Weisenhorn DM (1997) Calretinin-immunoreactivity during postnatal development of the rat isocortex: A qualitative and quantitative study. Cereb Cortex 7:130–142.
  146. Schwark HD, Li J (2000) Distribution of neurons immunoreactive for calcium-binding proteins varies across areas of cat primary somatosensory cortex. Brain Res Bull 51:379–385.
  147. Sherwood CC, Broadfield DC, Holloway RL, Gannon PJ, Hof PR (2003a) Variability of Broca’s area homologue in African great apes: Implications for language evolution. Anat Rec 271A:276–285.
    External Resources
  148. Sherwood CC, Holloway RL, Erwin JM, Schleicher A, Zilles K, Hof PR (2004) Cortical orofacial motor representation in old world monkeys, great apes, and humans. I. Quantitative analysis of cytoarchitecture. Brain Behav Evol 63:61–81.
    External Resources
  149. Sherwood CC, Lee PH, Rivara C-B, Holloway RL, Gilissen EPE, Simmons RMT, Hakeem A, Allman JM, Erwin JM, Hof PR (2003b) Evolution of specialized pyramidal neurons in primate visual and motor cortex. Brain Behav Evol 61:28–44.
  150. Shinoda Y, Yakota JI, Futami T (1981) Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci Lett 23:7–12.
  151. Sloper JJ (1973) An electron microscope study of the termination of afferent connections to the primate motor cortex. J Neurocytol 2:361–368.
  152. Sloper JJ, Powell TP (1979a) A study of the axon initial segment and proximal axon of neurons in the primate motor and somatic sensory cortices. Phil Trans R Soc Lond B Biol Sci 285:173–197.
  153. Sloper JJ, Powell TP (1979b) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Phil Trans R Soc Lond B Biol Sci 285:199–226.
  154. Somogyi P (1977) A specific ‘axo-axonal’ interneuron in the visual cortex of the rat. Brain Res 136:345–350.
  155. Somogyi P (1979) An interneurone making synapses specifically on the axon initial segment of pyramidal cells in the cerebral cortex of the cat. J Physiol 296:18P-19P.
  156. Somogyi P, Soltesz I (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat’s visual cortex. Neuroscience 19:1051–1065.
  157. Somogyi P, Freund TF, Cowey A (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7:2577–2607.
  158. Somogyi P, Kisvarday ZF, Martin KA, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261–294.
  159. Spatz WB, Illing RB, Weisenhorn DM (1994) Distribution of cytochrome oxidase and parvalbumin in the primary visual cortex of the adult and neonate monkey, Callithrix jacchus. J Comp Neurol 339:519–534.
  160. Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330:238–271.
  161. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136.
    External Resources
  162. Stichel CC, Singer W, Heizmann CW, Norman AW (1987) Immunohistochemical localization of calcium-binding proteins, parvalbumin and calbindin-D 28k, in the adult and developing visual cortex of cats: A light and electron microscopic study. J Comp Neurol 262:563–577.
  163. Strick PL, Sterling P (1974) Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscopy study. J Comp Neurol 153:77–106.
  164. Tokuno H, Takada M, Nambu A, Inase M (1997) Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey. J Comp Neurol 389:34–48.
  165. Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298.
  166. Travers JB, Rinaman L (2002) Identification of lingual motor control circuits using two strains of pseudorabies virus. Neuroscience 115:1139–1151.
  167. Tsang YM, Chiong F, Kuznetsov D, Kasarskis E, Geula C (2000) Motor neurons are rich in non-phosphorylated neurofilaments: Cross-species comparison and alterations in ALS. Brain Res 861:45–58.
  168. Ulfig N (2002) Calcium-binding proteins in the human developing brain. Adv Anat Embryol Cell Biol 165:III–IX, 1–92.
  169. Van Brederode JF, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298: 1–22.
  170. van der Gucht E, Vandesande F, Arckens L (2001) Neurofilament protein: A selective marker for the architectonic parcellation of the visual cortex in adult cat brain. J Comp Neurol 441:345–368.
  171. van Hooff JARAM (1962) Facial expressions in higher primates. Symp Zool Soc Lond 8:97–125.
  172. van Hooff JARAM (1967) The facial displays of catarrhine monkeys and apes. In: Primate Ethology (Morris D, ed), pp 7–68. Chicago: Aldine.
  173. Vogt BA, Pandya DN (1978) Cortico-cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey. J Comp Neurol 177:179–191.
  174. Volgui B, Pollak E, Buzas P, Gabriel R (1997) Calretinin in neurochemically well-defined cell populations of rabbit retina. Brain Res 763:79–86.
  175. Waters RS, Samulack DD, Dykes RW, McKinley PA (1990) Topographic organization of baboon primary motor cortex: Face, hand, forelimb, and shoulder representation. Somatosens Mot Res 7:485–514.
  176. West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497.
  177. Woolsey CN, Settlage PH, Meyer DR, Sencer W, Hamuy TP, Travis AM (1952) Patterns of localization in precentral and ‘supplementary’ motor areas and their relation to the concept of a premotor area. Res Pub Assoc Res Nerv Ment Dis 30:238–264.
  178. Xu Z, Marszalek JR, Lee MK, Wong PC, Folmer J, Crawford TO, Hsieh ST, Griffin JW, Cleveland DW (1996) Subunit composition of neurofilaments specifies axonal diameter. J Cell Biol 133:1061–1069.
  179. Yoshioka T, Levitt JB, Lund JS (1992) Intrinsic lattice connections of macaque monkey visual cortical area V4. J Neurosci 12:2785–2802.
  180. Yumiya H, Ghez C (1984) Specialized subregions in the cat motor cortex: Anatomical demonstration of differential projections to rostral and caudal sectors. Exp Brain Res 53:259–276.
  181. Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: July 01, 2003
Accepted: August 27, 2003
Published online: February 06, 2004
Issue release date: February 2004

Number of Print Pages: 25
Number of Figures: 13
Number of Tables: 4

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.