Forebrain neuroanatomy of the neonatal and juvenile dolphin (T. truncatus and s. coeruloalba)

Frontiers in Neuroanatomy

Volumn 9, Issue November, 2015, Pages 1-19

  Parolisi, Roberta ^a   Peruffo, Antonella ^b   Messina, Silvia ^a   Panin, Mattia ^b   Montelli, Stefano ^b   Giurisato, Maristella ^b   Cozzi, Bruno ^b   Bonfanti, Luca ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Bottlenose dolphin; Cerebellum; Germinative layers; Lateral ventricle; Postnatal brain development; Striatum; Striped dolphin; Thalamus

Indexed keywords

ADOLESCENT; ADULT; BASAL GANGLION; CELL DENSITY; DEVELOPMENTAL STAGE; DOLPHIN; FOREBRAIN; GRANULE CELL; GRAY MATTER; JUVENILE; MYELINATION; NEUROANATOMY; NEWBORN; SPECIES; STENELLA; TURSIOPS TRUNCATUS;

EID: 84948752050     PISSN: 16625129     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2015.00140     Document Type: Article

References (61)

1. Abraham, H., Tornoczky, T., Kosztolanyi, G., and Seress, L. (2001). Cell formation in the cortical layers of the developing human cerebellum. Int. J. Dev. Neurosci.19, 53-62. doi: 10.1016/S0736-5748(00)00065-4
2. Altman, J. (1969). Autoradiographic and histological studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J. Comp. Neurol. 137, 433-458.
3. Ballarin, C., Papini, L., Bortolotto, A., Butti, C., Peruffo, A., Sassu, R., et al.(2005). An on-line bank for marine mammals of the Mediterranean Sea and adjacent waters. Hystrix Ital. J. Mammal. 16, 127-133. doi: 10.4404/hystrix-16. 2-4350
4. Bearzi, G., Bonizzoni, S., Agazzi, S., and Gonzalvo, J. (2011). Striped dolphins and short-beaked common dolphins in the Gulf of Corinth, Greece: abundance estimates from dorsal fin photographs. Mar. Mamm. Sci. 27, E165-E184. doi:10.1111/j.1748-7692.2010.00448.x
5. Bonfanti, L., and Peretto, P. (2011). Adult neurogenesis in mammals-a theme with many variations. Eur. J. Neurosci. 34, 930-950. doi: 10.1111/j.1460-9568.2011.07832.x
6. Bonfanti, L., and Ponti, G. (2008). Adult mammalian neurogenesis and the New Zealand white rabbit. Vet. J. 175, 310-331. doi: 10.1016/j.tvjl.2007.01.023
7. Bonner, J. T. (1980). The Evolution of Culture in Animals. Princeton, NJ: Princeton University Press.
8. Buhl, E. H., and Oelschläger, H. A. (1986). Ontogenetic development of the nervus terminalis in toothed whales. Evidence for its non-olfactory nature. Anat.Embryol. (Berl.) 173, 285-294. doi: 10.1007/BF00318911
9. Butti, C., Janeway, C. M., Townshend, C., Wicinski, B. A., Reidenberg, J. S., Ridgway, S. H., et al. (2014). The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Brain Struct. Funct. 220, 3339-3368. doi:10.1007/s00429-014-0860-3
10. Cagnolaro, L., Cozzi, B., Notarbartolo di Sciara, G., and Podestà, M. (2015). Fauna d’Italia. XLIX-Mammalia IV. Cetacea, Calderini. Bologna: Edagricole – New Business Media, 1-376.
11. Cozzi, B., Podestà, M., Vaccaro, C., Poggi, R., Mazzariol, S., Huggenberger, S., et al. (2015). Precocious ossification of the tympanoperiotic bone in fetal and newborn dolphins: an evolutionary adaptation to the aquatic environment? Anat. Rec. (Hoboken) 298, 1294-1300. doi: 10.1002/ar.23120
12. Del Bigio, M. R. (2011). Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain 134, 1344-1361.doi: 10.1093/brain/awr052
13. Demski, L. S., Ridgway, S. H., and Schwanzel-Fukuda, M. (1990). The terminal nerve of dolphins: gross structure, histology and luteinizing-hormonereleasing hormone immunocytochemistry. Brain Behav. Evol. 36, 249-261. doi:10.1159/000115311
14. Fields, R. D. (2008). White matter in learning, cognition and psychiatric disorders. Trends Neurosci. 31, 361-370. doi: 10.1016/j.tins.2008.04.001
15. Furutani, R. (2008). Laminar and cytoarchitectonic features of the cerebral cortex in the Risso’s dolphin (Grampus griseus), striped dolphin (Stenellacoeruleoalba), and bottlenose dolphin (Tursiops truncatus). J. Anat. 213, 241- 248. doi: 10.1111/j.1469-7580.2008.00936.x
16. Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurol. Res. 1, 203-209.
17. Garey, L. J., and Leuba, G. (1986). A quantitative study of neuronal and glial numerical density in the visual cortex of the bottlenose dolphin: evidence for a specialized subarea and changes with age. J. Comp. Neurol. 247, 491-496. doi:10.1002/cne.902470408
18. Hof, P. R., Chanis, R., and Marino, L. (2005). Cortical complexity in cetacean brains. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1142-1152. doi:10.1002/ar.a.20258
19. Jacobs, M. S., McFarland, W. L., and Morgane, P. J. (1979). The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe(Rhinencephalon): the archicortex. Brain Res. Bull. 4, 1-108.
20. Jefferson, T. A., Webber, M. A., and Pitman, R. L. (2015). Marine Mammals of the World: A Comprehensive Guide to Their Identification, 2nd Edn. San Diego, CA:Academic Press, 1-616.
21. Kern, A., Siebert, U., Cozzi, B., Hof, P. R., and Oelschläger, H. H. A. (2011). Stereology of the neocortex in Odontocetes: qualitative, quantitative, and functional implications. Brain Behav. Evol. 77, 79-90. doi: 10.1159/000323674
22. Lesch, P. (1969). The development of the neutral lipids and fatty acids in the brain of man, whales and dolphins. Clin. Chim. Acta 25, 269-282. doi: 10.1016/0009-8981(69)90265-4
23. Liste, F., Palacio, J., Ribes, V., Alvarez-Clau, A., Domínguez, L. F., and Corpa, J. M. (2006). Anatomic and computed tomographic atlas of the head of the newborn bottlenose dolphin (Tursiops truncatus). Vet. Radiol. Ultrasound 47, 453-460. doi: 10.1111/j.1740-8261.2006.00167.x
24. Lois, C., and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148. doi: 10.1126/science.8178174
25. Marino, L. (1997). The relationship between gestation length, encephalization, and body weight in odontocetes. Mar. Mamm. Sci. 13, 133-138. doi: 10.1111/j.1748-7692.1997.tb00616.x
26. Marino, L., Sudheimer, K. D., Murphy, T. L., Davis, K. K., Pabst, D. A., McLellan, W. A., et al. (2001a). Anatomy and three-dimensional reconstructions of the brain of a Bottlenose dolphin (Tursiops truncatus) from magnetic resonance images. Anat. Rec. 264, 397-414. doi: 10.1002/ar.10018
27. Marino, L., Murphy, T. L., Gozal, L., and Johnson, J. I. (2001b). Magnetic resonance imaging and three-dimensional reconstructions of the brain of a fetal common dolphin, Delphinus delphis. Anat. Embryol. 203, 393-402. doi:10.1007/s004290100167
28. Marino, L., Sudheimer, K., Pabst, D. A., McLellan, W. A., Arshad, S., Naini, G., et al. (2004a). Anatomical description of an infant Bottlenose dolphin (Tursiopstruncatus) brain from magnetic resonance images. Aquat. Mamm. 30, 315-326. doi: 10.1578/AM.30.2.2004.315
29. Marino, L., Sudheimer, K., McLellan, W. A., and Johnson, J. I. (2004b).Neuroanatomical structure of the spinner dolphin (Stenella longirostrisorientalis) brain from magnetic resonance images. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 279, 601-610. doi: 10.1002/ar.a.20047
30. Montie, E. W., Schneider, G. E., Ketten, D. R., Marino, L., Touhey, K. E., and Hahn, M. E. (2007). Neuroanatomy of the subadult and fetal brain of the atlantic white-sided Dolphin (Lagenorhynchus acutus) from in situ magnetic resonance images. Anat. Rec. (Hoboken) 290, 1459-1479. doi: 10.1002/ar.20612
31. Montie, E. W., Schneider, G. E., Ketten, D. R., Marino, L., Touhey, K. E., and Hahn, M. E. (2008). Volumetric neuroimaging of the atlantic white-sided Dolphin(Lagenorhynchus acutus) brain from in situ magnetic resonance images. Anat. Rec. (Hoboken) 291, 263-282. doi: 10.1002/ar.20654
32. Mortensen, H. S., Pakkenberg, B., Dam, M., Dietz, R., Sonne, C., Mikkelsen, B., et al. (2014). Quantitative relationship in delphinid neocortex. Front. Neuroanat.8:132. doi: 10.3389/fnana.2014.00132
33. Oelschläger, H. A., Buhl, E. H., and Dann, J. F. (1987). Development of the nervus terminalis in mammals including toothed whales and humans. Ann. N. Y. Acad.Sci. 519, 447-464. doi: 10.1111/j.1749-6632.1987.tb36316.x
34. Oelschläger, H. H., Haas-Rioth, M., Fung, C., Ridgway, S. H., and Knauth, M. (2008). Morphology and evolutionary biology of the dolphin (Delphinus sp.)brain-MR imaging and conventional histology. Brain Behav. Evol. 71, 68-86. doi: 10.1159/000110495
35. Oelschläger, H. H. A., and Oelschläger, J. S. (2009). "Brain," in Encyclopedia of Marine Mammals, 2nd Edn, eds W. F. Perrin, B. Würsin, and J. G. M. Thewissen(San Diego, CA: Academic Press), 134-149.
36. O’Rahilly, R. (1972). Guide to staging of human embryos. Anat. Anz. 130, 556-559.
37. Patzke, N., Spocter, M. A., Karlsson, K. Æ, Bertelsen, M. F., Haagensen, M, Chawana, R., et al. (2015). In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct. Funct. 220, 361-383. doi: 10.1007/s00429-013-0660-1
38. Peretto, P., Giachino, C., Aimar, P., Fasolo, A., and Bonfanti, L. (2005). Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J. Comp. Neurol. 487, 407-427. doi:10.1002/cne.20576
39. Peruffo, A., and Cozzi, B. (2014). Bovine brain: an in vitro translational model in developmental neuroscience and neurodegenerative research. Front. Pediatr.2:74. doi: 10.3389/fped.2014.00074
40. Pilleri, G., and Gihr, M. (1970). The central nervous system of the Mysticete and Odontocete whales. Invest. Cet. 2, 89-128.
41. Pilleri, G., Peixun, C., and Zuohua, S. (1980). Concise Macroscopical Atlas of the Brain of the Common Dolphin (Delphinus delphis Linnaeus, 1758). WaldauBerne: Brain Anatomy Institute, University of Berne.
42. Pirlot, P., and Kamiya, T. (1975). Comparison of ontogenetic brain growth in marine and coastal dolphins. Growth 39, 507-524.
43. Pirlot, P., and Kamiya, T. (1982). Embryonic brain-growth in a dolphin. Anat. Embryol. 164, 43-50. doi: 10.1007/BF00301877
44. Ponti, G., Aimar, P., and Bonfanti, L. (2006a). Cellular composition and cytoarchitecture of the rabbit subventricular zone (SVZ) and its extensions in the forebrain. J. Comp. Neurol. 498, 491-507. doi:10.1371/journal.pone.0002366
45. Ponti, G., Peretto, P., and Bonfanti, L. (2006b). A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev. Biol. 294,168-180. doi: 10.1016/j.ydbio.2006.02.037
46. Ponti, G., Crociara, P., Armentano, M., and Bonfanti, L. (2010). Adult neurogenesis without germinal layers: the "atypical" cerebellum of rabbits. Arch. Ital. Biol.148, 147-158.
47. Ponti, G., Peretto, P., and Bonfanti, L. (2008). Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS ONE 3:e2366. doi: 10.1371/journal.pone.0002366
48. Rauschmann, M. A., Huggenberger, S., Kossatz, L. S., and Oelschlager, H. H. A. (2006). Head morphology in perinatal dolphins: a window into phylogeny and ontogeny. J. Morphol. 267, 1295-1315. doi: 10.1002/jmor.10477
49. Ridgway, S. H. (1986). "Dolphin brain size," in Research on Dolphins, eds M. M. Bryden and R. Harrison (Oxford: Oxford Science Publications), 59-70.
50. Ridgway, S. H. (1990). "The central nervous system of the bottlenose dolphin," in The Bottlenose Dolphin, eds S. Leatherwood and R. R. Reeves (Waltham, MA:Academic Press), 69-97.
51. Ridgway, S. H., and Brownson, R. H. (1984). Relative brain sizes and cortical surface areas in odontocetes. Acta Zool. Fenn. 172, 149-152.
52. Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H. H., Wong, M., et al. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386. doi: 10.1038/nature10487
53. Sanchez-Villagra, M. R., and Sultan, F. (2002). The cerebellum at birth in therian mammals, with special reference to rodents. Brain Behav. Evol. 59, 101-113. doi:10.1159/000064158
54. Snaidero, N., and Simons, M. (2014). Myelination at a glance. J. Cell Sci. 127, 2999-3004. doi: 10.1242/jcs.151043
55. Štěrba, O., Klima, M., and Schildger, B. (2000). Embryology of dolphins - staging and ageing of embryos and fetuses of some cetaceans. Adv. Anat. Embryol. Cell Biol. 157, 1-133.
56. Sternberger, N. H., Itoyama, Y., Kies, M. W., and Webster, H. D. (1978). Myelin basic protein demonstrated immunocytochemically in oligodendroglia prior to myelin sheath formation. Proc. Natl. Acad. Sci. U.S.A. 75, 2521-2524. doi:10.1073/pnas.75.5.2521
57. Thewissen, J. G. M., and Heyning, J. (2007). "Embryogenesis and development in Stenella attenuata and other cetaceans," in Reproductive Biology and Phylogeny of Cetacea. Whales, Dolphins and Porpoises, ed. D. L. Miller (Enfield, NH: Science Publishers), 307-330.
58. Tramontin, A. D., Garcìa-Verdugo, J. M., Lim, D. A., and Alvarez-Buylla, A. (2003). Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb. Cortex 13, 580-587. doi: 10.1093/cercor/13.6.580
59. Vincze, A., Mazlo, M., Seress, L., Komoly, S., and Abraham, H. (2008).A correlative light and electron microscopic study of postnatal myelination in the murine corpus callosum. Int. J. Dev. Neurosci. 26, 575-584. doi:10.1016/j.ijdevneu.2008.05.003
60. Wang, C., Liu, F., Liu, Y. Y., Zhao, C. H., You, Y., Wang, L., et al. (2011). Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res. 21, 1534-1550. doi: 10.1038/cr.2011.83
61. Workman, A. D., Charvet, C. J., Clancy, B., Darlington, R. B., and Finlay, B. L. (2013). Modeling transformations of neurodevelopmental sequences across mammalian species. J. Neurosci. 33, 7368-7383. doi:10.1523/JNEUROSCI.5746-12.2013