Abstract
Both lineages of the modern monotremes have distinctive features in the cerebral cortex, but the developmental mechanisms that produce such different adult cortical architecture remain unknown. Similarly, nothing is known about the differences and/or similarities between monotreme and therian cortical development. We have used material from the Hill embryological collection to try to answer key questions concerning cortical development in monotremes. Our findings indicate that gyrencephaly begins to emerge in the echidna brain shortly before birth (crown-rump length 12.5 mm), whereas the cortex of the platypus remains lissencephalic throughout development. The cortices of both monotremes are very immature at the time of hatching, much like that seen in marsupials, and both have a subventricular zone (SubV) within both the striatum and pallium during post-hatching development. It is particularly striking that in the platypus, this region has an extension from the palliostriatal angle beneath the developing trigeminoreceptive part of the somatosensory cortex of the lateral cortex. The putative SubV beneath the trigeminal part of S1 appears to accommodate at least two distinct types of cell and many mitotic figures and (particularly in the platypus) appears to be traversed by large numbers of thalamocortical axons as these grow in. The association with putative thalamocortical fibres suggests that this region may also serve functions similar to the subplate zone of Eutheria. These findings suggest that cortical development in each monotreme follows distinct paths from at least the time of birth, consistent with a long period of independent and divergent cortical evolution.
References
1.
Abbie AA (1938): The excitable cortex in the monotremata. Aust J Exp Biol Med Sci 16:143–152.
2.
Abbie AA (1940): Cortical lamination in the monotremata. J Comp Neurol 72:429–467.
3.
Abdel-Mannan O, Cheung AFP, Molnár Z (2008): Evolution of cortical neurogenesis. Brain Res Bull 75:398–404.
4.
Ashwell KWS (2010): Cerebral cortex and claustrum/endopiriform complex; in Ashwell KWS (ed): The Neurobiology of Australian Marsupials. Cambridge, Cambridge University Press, pp 129–153.
5.
Ashwell KW, Hardman CD, Paxinos G (2004): The claustrum is not missing from all monotreme brains. Brain Behav Evol 64:223–241.
6.
Bohringer RC, Rowe MJ (1977): The organization of the sensory and motor areas of cerebral cortex in the platypus (Ornithorhynchus anatinus). J Comp Neurol 174:1–14.
7.
Burrell H (1927): The Platypus. Sydney, Angus and Robertson.
8.
Butler AB, Molnár Z, Manger P (2002): Apparent absence of the claustrum in monotremes: implications for forebrain evolution in amniotes. Brain Behav Evol 60:230–240.
9.
Camens AB (2010): Were early tertiary monotremes really all aquatic? Inferring paleobiology and phylogeny from a depauperate fossil record. Proc Natl Acad Sci USA 107:E12.
10.
Carney RSE, Bystron I, López-Bendito G, Molnár Z (2007): Comparative analysis of extra-ventricular mitoses at early stages of cortical development in rat and human. Brain Struct Funct 212:37–54.
11.
Charvet CJ, Owerkowicz T, Striedter GF (2009): Phylogeny of the telencephalic subventricular zone in sauropsids: evidence for the sequential evolution of pallial and subpallial subventricular zones. Brain Behav Evol 73:285–294.
12.
Charvet CJ, Striedter GF (2011): Causes and consequences of expanded subventricular zones. Eur J Neurosci 34:988–993.
13.
Cheung AFP, Kondo S, Abdel-Mannan O, Chodroff RA, Sirey TM, Bluy LE, Webber N, DeProto J, Karlen SJ, Krubitzer L, Stolp HB, Saunders NR, Molnár Z (2010): The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb Cortex 20:1071–1081.
14.
Cheung AFP, Pollen AA, Tavare A, DeProto J, Molnár Z (2007): Comparative aspects of cortical neurogenesis in vertebrates. J Anat 211:164–176.
15.
De Carlos JA, O’Leary DD (1992): Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 12:1194–1211.
16.
Hassiotis M, Paxinos G, Ashwell KWS (2004): Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus). I. Areal organization. J Comp Neurol 475:495–517.
17.
Hassiotis M, Paxinos G, Ashwell KWS (2005): Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus). II. Laminar organization and synaptic density. J Comp Neurol 482:94–122.
18.
Hawkins M, Battaglia A (2009): Breeding behaviour of the platypus (Ornithorhynchus anatinus) in captivity. Aust J Zool 57:283–293.
19.
Hines M (1929): The brain of Ornithorhynchus anatinus. Phil Trans Royal Soc B Biol Sci 217:155–288.
20.
Holland N, Jackson SM (2002): Reproductive behaviour and food consumption associated with the captive breeding of platypus (Ornithorhynchus anatinus). J Zool (Lond) 256:279–288.
21.
Hughes RL, Carrick FN, Shorey CD (1975): Reproduction in the platypus Ornithorhynchus anatinus with particular reference to the evolution of viviparity. J Reprod Fertil 43:374–375.
22.
Iggo A, Gregory JE, Proske U (1992): The central projection of electrosensory information in the platypus. J Physiol 447:449–465.
23.
Jones EG (2009): The origins of cortical interneurons: mouse versus monkey and human. Cereb Cortex 19:1953–1956.
24.
Kriegstein A, Noctor S, Martinez-Cerdeno V (2006): Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7:883–890.
25.
Krubitzer L, Manger P, Pettigrew J, Calford M (1995): Organization of somatosensory cortex in monotremes: in search of the prototypical plan. J Comp Neurol 351:261–306.
26.
Lende RA (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.
27.
Manger PR, Calford MB, Pettigrew JD (1996): Properties of electrosensory neurons in the cortex of the platypus (Ornithorhynchus anatinus): implications for processing of electrosensory stimuli. Proc R Soc Lond B 263:611–617.
28.
Manger PR, Hall LS, Pettigrew JD (1998): The development of the external features of the platypus (Ornithorhynchus anatinus). Philos Trans R Soc Lond B Biol Sci 353:1115–1125.
29.
Marotte LR, Sheng X (2000): Neurogenesis and identification of developing layers in the visual cortex of the wallaby (Macropus eugenii). J Comp Neurol 416:131–142.
30.
McConnell SK, Ghosh A, Shatz CJ (1989): Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:978–982.
31.
Molnár Z (2011): Evolution of cerebral cortical development. Brain Behav Evol 78:94–107.
32.
Montiel JF, Wang WZ, Oeschger FM, Hoerder-Suabedissen A, Tung WL, Garcia-Moreno F, Holm IE, Villalón A, Molnár Z (2011): Hypothesis on the dual origin of the mammalian subplate. Front Neuroanat 5:25.
33.
Morrow G, Andersen NA, Nicol SC (2009): Reproductive strategies of the short-beaked echidna – a review with new data from a long-term study on the Tasmanian subspecies (Tachyglossus aculeatus setosus). Aust J Zool 57:275–282.
34.
Murakami F, Tanaka D, Yanagida M, Yamakazi E (2007): Intracortical multidirectional migration of cortical interneurons. Novartis Found Symp 288:116–125.
35.
Musser AM (2003): Review of the monotreme fossil record and comparison of paleontological and molecular data. Comp Biochem Physiol A Mol Integr Physiol 136:927–942.
36.
Musser AM, Archer M (1998): New information about the skull and dentary of the Miocene platypus Obdurodon dicksoni, and a discussion of ornithorhynchid relationships. Phil Trans R Soc Lond B Biol Sci 353:1063–1079.
37.
Nadarajah B, Alifragis P, Wong ROL, Parnavelas JG (2003): Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex 13:607–611.
38.
Nadarajah B, Parnavelas JG (2002): Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423–432.
39.
O’Brien SJ (2009): Comparative genomics in vertebrates: a role for the platypus. Aust J Zool 57:vii–ix.
40.
Pettigrew JD (1999): Electroreception in monotremes. J Exp Biol 202:1447–1454.
41.
Phillips MJ, Bennett TH, Lee MSY (2009): Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proc Natl Acad Sci USA 106:17089–17094.
42.
Pridmore PA, Rich TH, Vickers-Rich P, Gambaryan PP (2005): A tachyglossid-like humerus from the early Cretaceous of south-eastern Australia. J Mammal Evol 12:359–378.
43.
Puzzolo E, Mallamaci A (2010): Cortico-cerebral histogenesis in the opossum Monodelphis domestica: generation of a hexalaminar neocortex in the absence of a basal proliferative compartment. Neural Dev 5:8.
44.
Renfree MB, Papenfuss AT, Shaw G, Pask AJ (2009): Eggs, embryos and the evolution of imprinting: insights from the platypus genome. Reprod Fertil Dev 21:935–942.
45.
Rismiller PD, McKelvey MW (2009): Activity and behaviour of lactating echidnas (Tachyglossus aculeatus multiaculeatus) from hatching of egg to weaning of young. Aust J Zool 57:265–273.
46.
Scheich H, Langner G, Tidemann C, Coles RB, Guppy A (1986): Electroreception and electrolocation in platypus. Nature 319:401–402.
47.
Semon R (1894): Zur Entwicklungsgeschichte der Monotremen. Zoologische Forschungsreisen in Australien. Denkschr Med Naturw Ges Jena 2:61–74.
48.
Wang WZ, Oeschger FM, Montiel JF, García-Moreno F, Hoerder-Suabedissen A, Krubitzer L, Ek CJ, Saunders NR, Reim K, Villalón A, Molnár Z (2011): Comparative aspects of subplate zone studied with gene expression in sauropsids and mammals. Cereb Cortex 21:2187–2203.
49.
Welker W, Lende RA (1980): Thalamocortical relationships in echidna (Tachyglossus aculeatus); in Ebbesson SOE (ed): Comparative Neurology of the Telencephalon. New York, Plenum, pp 449–481.
50.
Zeller U (1989): Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus: (Mammalia, Prototheria, Monotremata). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft. Frankfurt am Main, W. Kramer.
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