Abstract
We have used Valverde-Golgi and Golgi-Colonnier techniques to analyze cortical neuronal morphology in four regions (frontal cortex, primary motor cortex, primary somatosensory cortex, primary visual cortex) of the isocortex of the echidna (Tachyglossus aculeatus). Eight classes of neurons could be identified – pyramidal, spinous bipolar, aspinous bipolar, spinous bitufted, aspinous bitufted, spinous multipolar, aspinous multipolar and neurogliaform. All except the pyramidal neurons were morphologically similar to neuronal classes seen in eutherian and metatherian isocortex. Pyramidal neurons made up a small proportion of all cortical neurons encountered in our preparations of echidna cortex (34% in visual cortex, 35% in somatosensory cortex, 41% in frontal cortex and 49% in motor cortex) compared to both reported values in eutherian cortex and values we found in rat cortex impregnations prepared in an identical fashion to the echidna material (75% in rat motor and 78% in rat somatosensory cortex). Many pyramidal neurons in the echidna isocortex were atypical (30–42% depending on region) with inverted somata, short or branching apical dendrites and/or few basal dendrites, very different from the usual pyramidal neuron morphology in eutherian cortex. Dendritic spine density on apical and basal dendrites of echidna pyramidal neurons in somatosensory cortex and apical dendrites of motor cortex pyramidal neurons was also lower than that found in the rat. The present findings are consistent with both pyramidal neurons and the many diverse types of non-pyramidal neurons having already emerged as discrete morphological entities very early in mammalian cortical evolution, at the time of divergence of the therian and prototherian lineage.
References
1.
Abbie, A.A. (1940) Cortical lamination in the monotremata. J. Comp. Neurol., 72: 429–467.
2.
Blaesing, B., M. Nossoll, G. Teuchert-Noodt, and R.R. Dawirs (2001) Postnatal maturation of prefrontal pyramidal neurons is sensitive to a single early dose of methamphetamine in gerbils (Meriones unguiculatus). J. Neural. Trans., 108: 101–113.
3.
Blümcke, I., P.R. Hof, J.H. Morrison, and M.R. Celio (1990) Distribution of parvalbumin imunoreactivity in the visual cortex of old world monkeys and humans. J. Comp. Neurol., 301: 417–432.
4.
Clemens, W.A. (1970) Mesozoic mammalian evolution. Ecol. Syst., 1: 357–390.
5.
Clemens, W.A. (1979) Notes on the monotremata. In Mesozoic Mammals: The First Two-thirds of Mammalian Evolution (ed. by J.A. Lillegraven, Z. Kielan-Jaworowska and W.A. Clemens), University of California Press, Berkeley, CA, pp. 309–311.
6.
Connor, J.R., S.E. Beban, P.A. Hopper, B. Hansen, and M.C. Diamond (1982) A Golgi study of the superficial pyramidal cells in the somatosensory cortex of socially reared old adult rats. Exp. Neurol., 76: 35–45.
7.
Dann, J. F., and E.H. Buhl (1995) Patterns of connectivity in the neocortex of the echidna (Tachyglossus aculeatus). Cerebr. Cortex, 5: 363–373.
8.
De Felipe, J., and E.G. Jones (1992) High-resolution light and electron microscopic immunocytochemistry of colocalized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. Eur. J. Neurosci. 4:46–60.
9.
De Felipe, J., S.H.C. Hendry, and E.G. Jones (1989) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res., 503: 49–54.
10.
De Felipe, J., S.H.C. Hendry, T. Hashikawa, M. Molinari, and E.G. Jones (1990) A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience, 37: 655–673.
11.
Deschênes, M., A. Labelle, and P. Landry (1979) Morphological characterization of slow and fast pyramidal tract cells in the rat. Brain Res., 178: 251–274.
12.
Divac, I., M.C. Holst, J. Nelson, and J.S. McKenzie (1987a) Afferents of the frontal cortex in the echidna (Tachyglossus aculeatus). Indication of an outstandingly large prefrontal area. Brain Behav. Evol., 30: 303–320.
13.
Divac, I, J.D. Pettigrew, M.C. Holst, and J.S. McKenzie (1987b) Efferent connections of the prefrontal cortex of the echidna (Tachyglossus aculeatus). Brain Behav. Evol., 30: 321–327.
14.
Fairén, A, J, De Felipe and J. Regidor (1984) Nonpyramidal neurons. General account. In Cerebral Cortex Vol. 1. Cellular Components of the Cerebral Cortex (ed by A. Peters and E.G. Jones), Plenum Press, New York, pp. 201–253.
15.
Feldman, M.L. (1984) Morphology of the neocortical pyramidal neuron. In Cerebral Cortex Vol. 1. Cellular Components of the Cerebral Cortex (ed by A. Peters and E.G. Jones), Plenum Press, New York, pp. 123–200.
16.
Feldman, M.L., and A. Peters (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J. Comp. Neurol., 179: 761–794.
17.
Feldman, M.L., and A. Peters (1979) A technique for estimating total spine numbers on Golgi impregnated dendrites. J. Comp. Neurol., 188: 527–542.
18.
Galofré, E., and I. Ferrer (1987) Development of dendritic spines in the Vth’s layer pyramidal neurons of the rat’s somatosensory cortex. A qualitative and quantitative study with the Golgi method. J. Hirnforsch., 28: 653–659.
19.
Garey, L.J., E. Winkelmann, and K. Brauer (1985) Golgi and Nissl studies of the visual cortex of the bottlenosed dolphin. J. Comp. Neurol., 240: 305–321.
20.
Glezer, I.I., and P.J. Morgane (1990) Ultrastructure of synapses and Golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale. Brain Res. Bull., 24: 401–427.
21.
Glezer, I.I., P.R. Hof, and P.J. Morgane (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.
22.
Hestrin, S., and W.E. Armstrong (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci., 16: 5290–5300.
23.
Hof, P.R., I.I. Glezer, F. Condé, R.A. Flagg, M.B. Rubin, E.A. Nimchinsky, and D.M. Vogt Weisenhorn (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.
24.
Hof, P.R., I.I. Glezer, E.A. Nimchinsky, and J.M. Erwin (2000) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: Evidence from primates, cetaceans and artiodactyls. Brain Behav. Evol., 55: 300–310.
25.
Horner, C.H. (1993) Plasticity of the dendritic spine. Prog. Neurobiol., 41: 281–321.
26.
Jones, E.G. (1975) Varieties and distribution of non-pyramidal cells in somatic sensory cortex of the squirrel monkey. J. Comp. Neurol., 160: 205–268.
27.
Kawaguchi, Y. (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci., 15: 2638–2655.
28.
Krubitzer, L., P. Manger, J. Pettigrew, and M. Calford (1995) Organization of somatosensory cortex in monotremes: In search of the prototypical plan. J. Comp. Neurol., 351: 261–306.
29.
Lende, R.A. (1964) Representation in the cerebral cortex of a primitive mammal, sensorimotor, visual, and auditory fields in the echidna (Tachyglossus aculeatus). J. Neurophysiol., 27: 37–48.
30.
Lund, J.S., and D.A. Lewis (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J. Comp. Neurol., 328: 282–312.
31.
Mathers, L.H., Jr (1979) Postnatal development in the rabbit visual cortex. Brain Res., 168: 21–29.
32.
Meyer, G. (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J. Comp. Neurol., 262: 402–428.
33.
Miller, M.W. (1986) Maturation of rat visual cortex. III. Postnatal morphogenesis and synpatogenesis of local circuit neurons. Brain Res. Dev. Brain Res., 25: 271–285.
34.
Mrzljak L., U.B. Uylings, I. Kostovic, and C.G. Van Eden (1988) Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study. J. Comp. Neurol., 271: 355–386.
35.
Nieuwenhuys, R. (1994) The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat. Embryol., 190: 307–337.
36.
Paxinos, G., L. Kus, K.W.S. Ashwell, and C. Watson (1999) Chemoarchitectonic Atlas of the Rat Forebrain. Academic Press, San Diego, CA.
37.
Peters, A. (1984) Bipolar cells. In Cerebral Cortex Vol. 1. Cellular Components of the Cerebral Cortex (ed by A. Peters and E.G. Jones), Plenum Press, New York, pp. 381–407.
38.
Peters, A., and A. Fairén (1978) Smooth and sparsely-spined stellate cells in the visual cortex of the rat: A study using a combined Golgi-Electron microscope technique. J. Comp. Neurol., 181: 129–172.
39.
Peters, A., and L.M. Kimerer (1981) Bipolar neurons in rat visual cortex: a combined Golgi-electron microscope study. J. Neurocytol., 10: 921–946.
40.
Peters, A., and J. Regidor (1981) A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex. J. Comp. Neurol., 203: 685–716.
41.
Petit, T.L., J.C. Le Boutillier, A. Gregorio, and H. Libstug (1988) The pattern of dendritic development in the cerebral cortex of the rat. Brain Res. Dev. Brain Res., 41: 209–219.
42.
Quiroga, J.C. (1980a) The brain of the mammal-like reptile Probainognathus jenseni (Therapsida, Cynodontia). A correlative paleo-neoneurological approach to the neocortex at the reptile-mammal transition. J. Hirnforsch., 21: 299–336.
43.
Quiroga, J.C. (1980b) Further studies on cynodont endocasts (Reptilia-Therapsida). Z. Mikrosk. Anat. Forsch., 94: 580–592.
44.
Sanides, D., and F. Sanides (1974) A comparative Golgi study of the neocortex in insectivores and rodents. Z. Mikrosk. Anat. Forsch., 88: 957–977.
45.
Simons, D.J., and T.A. Woolsey (1984) Morphology of Golgi-Cox impregnated barrel neurons in rat SmI cortex. J. Comp. Neurol., 230: 119–132.
46.
Somogyi P., and A. Cowey (1981) Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J Comp Neurol., 195: 547–566.
47.
Somogyi, P., Z.F. Kisvárday, T.F. Freund, and A. Cowey (1984) Characterization by Golgi impregnation of neurons that accumulate 3H-GABA in the visual cortex of monkey. Exp. Brain Res., 53: 295–303.
48.
Tyler, C.J., S.A. Dunlop, R.D. Lund, A.M. Harman, J.F. Dann, L.D. Beazley, and J.S. Lund (1998) Anatomical comparison of the macaque and marsupial visual cortex: Common features that may reflect retention of essential cortical elements. J. Comp. Neurol., 400: 449–468.
49.
Ulinski, P.S. (1984) Thalamic projections to the somatosensory cortex of the echidna (Tachyglossus aculeatus). J. Comp. Neurol., 229: 153–170.
50.
Valverde, F (1970) The Golgi method. A tool for comparative structural analysis. In Contemporary Research Methods in Neuroanatomy (ed. by W.J.H. Nauta and S.O.E. Ebbesson), Springer-Verlag, New York, pp. 12–31.
51.
Valverde, F., and M.V. Facal-Valverde (1986) Neocortical layers I and II of the hedgehog (Erinaceus europaeus) I. intrinsic organization. Anat. Embryol., 173: 413–430.
52.
Walsh, T.M., and F.F. Ebner (1970) The cytoarchitecture of somatic sensory-motor cortex in the opossum (Didelphis marsupialis virginiana): A Golgi study. J. Anat., 107: 1–18.
53.
Welker,W., and R.A. Lende (1980) Thalamocortical relationship in echidna (Tachyglossus aculeatus). In Comparative Neurology of the Telencephalon (ed. by S.O.E Ebbesson), Plenum Press, New York, pp. 449–481.
54.
Zervas, M., and S.U. Walkley (1999) Ferret pyramidal cell dendritogenesis: Changes in morphology and ganglioside expression during cortical development. J. Comp. Neurol., 413: 429–448.
© 2003 S. Karger AG, Basel
2003
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.
You do not currently have access to this content.
