Abstract
An account of work performed at the UNA laboratories since 1992 on the detection and description of interlaminar glial processes, is presented. The incidental observation (serendipity) of longer than expected glial processes in the superficial layers of the cerebral cortex in hemiparkinsonian Cebus apella monkeys, was expanded afterwards to cover the largest possible sampling of representatives of mammalian orders and species, as well as in experimental and pathological conditions, in human and non-human primates. The term interlaminar was coined to differentiate these processes from the classical astroglial stellate, intralaminar ones. Such account grew to the point of inspiring, on speculative grounds, possible roles in the organization of the cerebral cortex. Interlaminar glial processes represent an essentially primate characteristic, affected by neuropathological conditions such as DS and AD and experimental procedures affecting normal sensory input, suggesting thalamic involvement in their normal expression. Their ontogenetic development, phylogenetic evolution and aging changes are described.
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Abbreviations
- IR:
-
Immunoreactivity/immunoreactive
- IGP:
-
Interlaminar glial processes
- DS:
-
Down’s syndrome
- AD:
-
Alzheimer’s disease
- AE:
-
Albert Einstein
References
Allen NJ, Barres BA (2005) Signaling between glia and neurons: focus on synaptic plasticity. Curr Opin Neurobiol 15:542–548
Anderson B (1999) Commentary. A proof of the need for the spatial clustering of interneuronal connections to enhance cortical computation. Cereb Cortex 9:2–3
Andriezen WL (1893) The neuroglia elements of the brain. Brit Med J 29:227–230
Araque A, Parpura V, Sanzqiri RP, Haydon PG (1999) Tripartite synapses: glia the unacknowledged partner. TINS 22:208–215
Barres BA, Koroshetz WJ, Chun LLY, Corey DP (1990) Ion channel expression by white matter glia: the type 1 astrocyte. Neuron 5:527–544
Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Ann Rev Neurosci 21:149–186
Cajal SR (1904) In: Textura del sistema nervioso del hombre y de los vertebrados vol 2, Pt. 2, chpt. 37, pp 792–864. Madrid:Moya, Spain
Casseb GI, Varner JE (1987) Immunocytolocalization of extensin in developing soybean seed coats by immunogold-silver staining and by tissue printing on nitrocellulose paper. J Cell Biol 105:2581–2588
Colombo JA (1994) Regional non-homogeneities in cortical astroglia in adult monkeys. Persistence of transitional forms. Proceedings of Society for Neuroscience 24th annual meeting 20 (2): 578.13, Miami, FL, USA
Colombo JA (1995) Interlaminar astroglial processes in the cerebral cortex of adult primates:further characterization. In: Proceed Ist Int Conference on Glial Contributions to Behaviour, pp 117–118, Belfast
Colombo JA (1996) Interlaminar astroglial processes in the cerebral cortex of adult monkeys but not of adult rats. Acta Anat (Basel) 155:57–62
Colombo JA (2000) Comentarios a propósito del cerebro de Albert Einstein. Medicina 60:530–532
Colombo JA (2001) A columnar-supporting mode of astroglial architecture in the cerebral cortex of adult primates. Neurobiology 9:1–16
Colombo JA, Puissant V (1994) Regional nonhomogeneities in cortical astroglia in adult monkeys. Persistence of transitiona forms. In: Annual Meeting-Society for Neuroscience abstract no 578.13, Miami, Fla
Colombo JA, Reisin HD (2004) Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res 1006:126–131
Colombo JA, Yáñez A, Puissant V, Lipina S (1995) Long, interlaminar astroglial cell processes in the cortex of adult monkeys. J Neurosci Res 40:551–556
Colombo JA, Yáñez A, Lipina S (1997a) Interlaminar astroglial processes in the cerebral cortex of non human primates: response to injury. J Brain Res 38:503–512
Colombo JA, Lipina S, Yáñez A, Puissant V (1997b) Postnatal development of interlaminar astroglial processes in the cerebral cortex of primates. Int J Dev Neurosci 15:823–833
Colombo JA, Gayol S, Yáñez A, Marco P (1997c) Immunocytochemical and electron microscope observations on astroglial interlaminar processes in the primate neocortex. J Neurosci Res 48:352–357
Colombo JA, Härtig W, Lipina S, Bons N (1998) Astroglial interlaminar processes in the cerebral cortex of prosimians and Old World monkeys. Anat Embryol 197:369–376
Colombo JA, Schleicher A, Zilles K (1999a) Patterned distribution of immunoreactive astroglial processes in the striate (V1) cortex of New World Monkeys. Glia 25:85–92
Colombo JA, Yáñez A, Lipina S (1999b) Disruption of patterns of immunoreactive glial fibrillary acidic protein processes in the Cebus apella striate cortex following loss of visual input. J Brain Res 4:449–453
Colombo JA, Fuchs E, Härtig 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 201:111–120
Colombo JA, Napp MI, Yáñez A, Reisin H (2001) Tissue printing of astroglial interlaminar processes from human and non-human primate cerebral cortex. Brain Res Bull 55:561–565
Colombo JA, Quinn B, Puissant V (2002) Disruption of astroglial interlaminar processes in Alzheimer’s disease. Brain Res Bull 58:235–242
Colombo JA, Sherwood C, Hof P (2004) Interlaminar astroglial processes in the cerebral cortex of great apes. Anat Embryol 429:391–394
Colombo JA, Reisin HD, Jones M, Bentham C (2005) Development of interlaminar astroglial processes in the cerebral cortex of control and Down’s syndrome human cases. Exp Neurol 193:207–217
Colombo JA, Reisin HD, Miguel-Hidalgo JJ, Rajkowska G (2006) Cerebral cortex astroglia and the brain of a genius: a propos of A. Einstein’s. Brain Res Rev 52:257–263
D’Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM II, Janigro D (1998) Functional hippocampal astrocytes. J Neurosci 18:4425–4438
DeFelipe J, Markram H, Rockland KS (2012) The neocortical column. Front Neuroanat 6:1–2
Dierig S (1994) Extending the neuron doctrine: carl Ludwig Schleich (1859–1922) and his reflections on neuroglia at the inception of the neural-network concept in 1894. TINS 17:449–452
Eilam R, Aharoni R, Arnon R, Malach R (2016) Astrocyte morphology is confined by cortical functional boundaries in mammals ranging from rats to humans. doi:10.7554/eLife.15915
Gaspar P, Colombo JA, Puissant V, Berger B (1992) Long term alterations of the aminergic innervations in MPTP-induced hemiparkinsonism in Cebus monkeys. Meet Europ Neurosci Ass, Amsterdam, The Netherlands
Gaspar P, Febret A, Colombo JA (1993) Serotoninergic sprouting in primate MPTP-induced hemiparkinsonism. Exp Brain Res 96:100–106
Gayol S, Pannicke T, Reichenbach A, Colombo JA (1999) Cell–cell coupling in cultures of striatal and cortical astrocyte of the monkey Cebus apella. J Brain Res 4:473–479
Giaume C, Liu X (2012) From a glial syncytium to a more restricted and specific glial networking. J Phys Paris 106:34–39
Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev 11:87–99
Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu O, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M (2013) Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12:342–353
Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2:185–193
Höfer T, Venance L, Giaume C (2002) Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J Neurosci 22:4850–4859
Hortega Del Rio (1942) La neuroglia normal. Conceptos de angiogliona y neurogliona. Arch Histol Normal Patol 1:5–71
Jones EG (2000) Commentary. Microcolumns in the cerebral cortex. PNAS 97:5019–5021
Jones EG (2001) The thalamic matrix and thalamocortical synchrony. TINS 24:595–601
Kettenmann H, Ransom B (2005) The concept of neuroglia: a historical perspective. In: Kettenman H, Ransom BR (eds) Neuroglia. Oxford University Press, Oxford, pp 1–16
Kufler SW (1967) Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on glial membrane potential. Proc R Soc B 168:1–28
Lanosa X, Reisin HD, Santacroce I, Colombo JA (2008) Astroglial dye-coupling: and in vitro analysis of regional interspecies differences in rodents and primates. Brain Res 1240:82–86
Lewis TJ, Rinzel J (2000) Self-organized synchronous oscillations in a network of excitable coupled gap junctions. Netw Comput Neural Syst 11:299–320
Martinotti C (1889) Contributo allo studio della corteccia cerebrale, ed all’origine centrale dei nervi. Ann Fren Sci Affin 1:314–332
Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434
Mountcastle VB (1974) Neural mechanisms in somesthesia. In: Mountcastle VB (ed) Medical physiology. The CV Mosby Co, St. Louis, pp 307–347
Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722
Mugnaini E (1986) Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In: Fedoroff S, Vernadakis A (eds) Astrocytes, vol 1. Academic Press Inc, NY, pp 329–371
Newman EA, Frambach DA, Odette LL (1984) Control of extracellular potassium by levels by retinal glial cell K+ siphoning. Science 225:1174–1175
Nicholson C, Sykova E (1998) Extracellular space structure revealed by diffusion analysis. Trends Neurosci 21:207–215
Oberheim NA, Takano T, Han X, He W, Lin JHC, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann GJ, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276–3287
Perea G, Navarrete M, Araque A (2009) A tripartite synapses: astrocyte process and control synaptic information. Trends Neurosci 32:421–431
Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176
Reichenbach A, Wolburg H (2005) Astrocytes and ependymal glia. In: Kettenman H, Ransom BR (eds) Neuroglia. Oxford University Press, Oxford
Reisin HD, Colombo JA (2002a) Considerations on the astroglial architecture and the columnar organization of the cerebral cortex. Cell Mol Neurobiol 22:633–644
Reisin HD, Colombo JA (2002b) Astroglial interlaminar processes in human cerebral cortex: variations in cytoskeletal profiles. Brain Res 937:51–57
Reisin H, Colombo JA (2004) Glial changes in primate cerebral cortex following long-term sensory deprivation. Brain Res 1000:179–182
Rempel-Clower NL, Barbas H (2000) The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cereb Cortex 10:851–865
Retzius G (1894) Die Neuroglia des Gehirns beim Menschen und bei Säugethieren. Biol Untersuchungen, Neue Folge 6: 1–28. Verlag, Jena
Ringo JL (1991) Neuronal interconnection as a function of brain size. Brain Behav Evol 38:1–6
Robertson JM (2014) Astrocytes and the evolution of the human brain. Med Hypoth 82:236–239
Rouach N, Koulakoff A, Giaume C (2004) Neurons set the tone of gap junctional communication in astrocytic networks. Neurochem Int 45:265–272
Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551–1555
Schenker NM, Buxhoeveden DP, Blackmon WL, Amunts K, Zilles K, Semendeferi K (2008) A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca’s area in humans and great apes. J Comput Neurol 510:117–128
Schipke CG, Kettenman H (2004) Astrocyte responses to neuronal activity. Glia 47:226–232
Schlaug G, Schleicher A, Zilles KJ (1995) Quantitative analysis of the columnar arrangement of neurons in the human cingulate cortex. Comput Neurol 351:441–452
Shiramatsu IT, Takahashi K, Noda T, Kanzaki R, Nakahara H, Takahashi A (2016) Microelectrode mapping of tonotopic, laminar and field’s specific organization of thalamo-cortical pathway in the rat. Neuroscience 332:38–52
Simonton DK (1999) “The origins of genius” (Darwinian perspectives on creativity). Oxford University Press, New York
Singer W (1995) Development and poasticity of cortical processing architectures. Science 270:758–763
Varon S, Somjen GG (1979) In: “Neuron-glia interactions” Neurosci Res Program Bull. 17:1–239. Boston-Mass
Verkhratsky A, Butt AM (2013) In: Verkhratsky A, Butt AM (eds) Glial physiology and pathophysiology. Wiley, NJ
Verkhratsky A, Nedergaard M (2016) The homeostatic astroglia emerges from evolutionary specialization of neural cells. Philos Trans R Soc B 371:20150428
Vernadakis A (1996) Glia-neuron intercommunications and synaptic plasticity. Progr Neurobiol 49:185–214
von Bonin G, Mehler WR (1971) On columnar arrangement of nerve cells in cerebral cortex. Brain Res 27:1–9
Acknowledgements
To my wife Beatriz for life-long encouragement and support; to all associates and laboratory assistants whose names are included in the corresponding publications, to Carlos Nagle MD and technicians working in the indoor primate facility of CIRHE (CEMIC-CONICET), to all donors of brain material (institutional Brain Tissue Banks and individual colleagues) from so many animal sources. Special thanks to Prof. Drs. Karl Zilles (Research Centre Jülich, Germany), Axel Schleicher (Dusseldorf, Germany), Andreas Reichenbach (Leipzig, Germany), Arthur Butt (Portland, G. Britain), Jean De Vellis (Los Angeles, USA), Javier DeFelipe (Instituto Cajal, Madrid, Spain), Eva Sykova (Prague, Czech Republic), Frank Kirchhoff (Homburg, Germany) and Marina Bentivoglio (Verona, Italy) for their support and productive criticism to our various published reports. My recognition for their most critical past financial support to the Alexander Humboldt Foundation (Germany), DAAD (Germany), supporters of Fundación Conectar, CONICET, CEMIC, Fundación N. Quirno, Lejeune Foundation (France), European Community, Fundación Bunge y Born and British Royal Society. I also wish to thank the Directors and personnel of the primate facility at CAPRIM (Corrientes, Argentina).
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Colombo, J.A. The interlaminar glia: from serendipity to hypothesis. Brain Struct Funct 222, 1109–1129 (2017). https://doi.org/10.1007/s00429-016-1332-8
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DOI: https://doi.org/10.1007/s00429-016-1332-8