Quantitative relationships in delphinid neocortex

Frontiers in Neuroanatomy

Volumn 8, Issue NOV, 2014, Pages

  Mortensen, Heidi S ^a,b   Pakkenberg, Bente ^a   Dam, Maria ^b   Dietz, Rune ^c   Sonne, Christian ^c   Mikkelsen, Bjarni ^d   Eriksen, Nina ^a  

^a FREDERIKSBERG HOSPITAL   (Denmark)

^b Research Department Environment Agency   (Iceland)

^c AARHUS UNIVERSITY   (Denmark)

^d Museum of Natural History   (Iceland)

Author keywords

Animal cognition; Glia neuron ratio; Neocortical cell density; Neocortical cell number; Stereology

Indexed keywords

ADULT; ANATOMICAL CONCEPTS; ANIMAL CELL; ARTICLE; AUDITORY CORTEX; BRAIN MAPPING; BRAIN REGION; BRAIN SIZE; BRAIN WEIGHT; CELL COUNTING; CELL DENSITY; DOLPHIN; GLIA CELL; HEMISPHERIC DOMINANCE; MALE; MATHEMATICAL MODEL; NEOCORTEX; NONHUMAN; STRIATE CORTEX; VISUAL CORTEX;

EID: 84930504768     PISSN: 16625129     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00132     Document Type: Article

References (80)

1. Baird, R. W., Borsani, J. F., Hanson, M. B., and Tyack, P. L. (2002). Diving and night-time behavior of long-finned pilot whales in the Ligurian Sea. Mar. Ecol. Prog. Ser. 237, 301-305. doi: 10.3354/meps237301
2. Busnel, R.-G., and Dziedzic, A. (1966). “Acoustic signals of the pilot whale Globicephala melaena and of the porpoises Delphinus delphis and Phocoena phocoena,” in Whales, Dolphins and Porpoises, ed K. S. Norris (Berkeley; Los Angeles, CA: University of California Press), 607-646.
3. Christensen, J. R., Larsen, K. B., Lisanby, S. H., Scalia, J., Arango, V., Dwork, A. J., et al. (2007). Neocortical and hippocampal neuron and glial cell numbers in the rhesus monkey. Anat. Rec. (Hoboken) 290, 330-340. doi: 10.1002/ar.20504
4. Delfour, F., and Marten, K. (2001). Mirror image processing in three marine mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus). Behav. Processes 53, 181-190. doi: 10.1016/S0376-6357(01)00134-6
5. Desportes, G., Saboureau, M., and Lacroix, A. (1993). Reproductive maturity and seasonality of male long-finned pilot whales, off the Faroe Islands. Rep. Int. Whal. Commn. (Special Issue 14), 233-262.
6. Dorph-Petersen, K. A., Gundersen, H. J., and Jensen, E. B. (2000). Non-uniform systematic sampling in stereology. J. Microsc. 200, 148-157. doi: 10.1046/j.1365-2818.2000.00750.x
7. Emery, N. J. (2006). Cognitive ornithology: the evolution of avian intelligence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 23-43. doi: 10.1098/rstb.2005.1736
8. Eriksen, N., and Pakkenberg, B. (2007). Total neocortical cell number in the mysticete brain. Anat. Rec. (Hoboken) 290, 83-95. doi: 10.1002/ar.20404
9. Eriksen, N., and Pakkenberg, B. (2014). “Comparative stereology studies of brains from marine mammals,” in Neurostereology, eds P. R. Mouton and A. Iowa (John Wiley & Sons, Inc.), 99-112.
10. Furutani, R. (2008). Laminar and cytoarchitectonic features of the cerebral cortex in the Risso’s dolphin (Grampus griseus), striped dolphin (Stenella coeruleoalba), and bottlenose dolphin (Tursiops truncatus). J. Anat. 213, 241-248. doi: 10.1111/j.1469-7580.2008.00936.x
11. 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
12. Gingerich, P. D., Wells, N. A., Russell, D. E., and Shah, S. M. (1983). Origin of whales in epicontinental remnant seas: new evidence from the early eocene of Pakistan. Science 220, 403-406. doi: 10.1126/science.220.4595.403
13. Glezer, I. (2002). “Neural Morphology,” in Marine Mammal Biology (An Evolutionary Approach), ed R. Hoezel (Oxford, UK: Blackwell Publishing), 98-115.
14. Glezer, I. I., Hof, P. R., Leranth, C., and Morgane, P. J. (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. doi: 10.1093/cercor/3.3.249
15. Glezer, I. I., Jacobs, M. S., and Morgane, P. J. (1988). Implications of the “initial brain” concept for brain evolution in Cetacea. Behav. Brain Sci. 11, 75-89. doi: 10.1017/S0140525X0005281X
16. Glezer, I. I., and Morgane, P. J. (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. doi: 10.1016/0361-9230(90)90096-I
17. Gundersen, H. J., Bendtsen, T. F., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., et al. (1988). Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96, 379-394. doi: 10.1111/j.1699-0463.1988.tb05320.x
18. Gundersen, H. J., and Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229-263. doi: 10.1111/j.1365-2818.1987.tb02837.x
19. Gundersen, H. J., Jensen, E. B., Kieu, K., and Nielsen, J. (1999). The efficiency of systematic sampling in stereology-reconsidered. J. Microsc. 193, 199-211. doi: 10.1046/j.1365-2818.1999.00457.x
20. Heide-Jørgensen, M. P., Bloch, D., Stefansson, E., Mikkelsen, B., Ofstad, L. H., and Dietz, R. (2002). Diving behaviour of long-finned pilot whales Globicephala melas around the Faroe Islands. Wildl. Biol. 8, 307-313.
21. Herculano-Houzel, S. (2011a). Brains matter, bodies maybe not: the case for exam- ining neuron numbers irrespective of body size. Ann. N.Y. Acad. Sci. 1225, 191-199. doi: 10.1111/j.1749-6632.2011.05976.x
22. Herculano-Houzel, S. (2011b). Not all brains are made the same: new views on brain scaling in evolution. Brain Behav. Evol. 78, 22-36. doi: 10.1159/000327318
23. Herculano-Houzel, S., Avelino-De-Souza, K., Neves, K., Porfirio, J., Messeder, D., Mattos Feijo, L., et al. (2014). The elephant brain in numbers. Front. Neuroanat. 8:46. doi: 10.3389/fnana.2014.00046
24. Herculano-Houzel, S., and Kaas, J. H. (2011). Gorilla and orangutan brains con- form to the primate cellular scaling rules: implications for human evolution. Brain Behav. Evol. 77, 33-44. doi: 10.1159/000322729
25. Herman, L. M. (2010). What laboratory research has told us about dolphin cognition. Int. J.Comp. Psychol. 23, 310-330.
26. Herman, L. M., Peacock, M. F., Yunker, M. P., and Madsen, C. J. (1975). Bottlenosed dolphin: duoble-split pupil yields equivalent aerial and underwater diurnal acuity. Science 1989, 650-659. doi: 10.1126/science.1162351
27. 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
28. Hof, P. R., and Van Der Gucht, E. (2007). Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat. Rec. (Hoboken) 290, 1-31. doi: 10.1002/ar.20407
29. Jaakkola, K., Fellner, W., Erb, L., Rodriguez, M., and Guarino, E. (2005). Understanding of the concept of numerically “less” by bottlenose dolphins (Tursiops truncatus). J. Comp. Psychol. 119, 296-303. doi: 10.1037/0735-7036.119.3.296
30. Jelsing, J., Nielsen, R., Olsen, A. K., Grand, N., Hemmingsen, R., and Pakkenberg, B. (2006). The postnatal development of neocortical neurons and glial cells in the Gottingen minipig and the domestic pig brain. J. Exp. Biol. 209, 1454-1462. doi: 10.1242/jeb.02141
31. Jerison, H. J. (1985). Animal Intelligence as encephaliztion. Phil. Trans. R. Soc. B 308, 21. doi: 10.1098/rstb.1985.0007
32. Karlsen, A. S., and Pakkenberg, B. (2011). Total numbers of neurons and glial cells in cortex and basal ganglia of aged brains with Down syndrome-a stereological study. Cereb. Cortex 21, 2519-2524. doi: 10.1093/cercor/bhr033
33. Keogh, M. J., and Ridgway, S. H. (2008). Neuronal fiber composition of the corpus callosum within some odontocetes. Anat. Rec. (Hoboken) 291, 781-789. doi: 10.1002/ar.20701
34. Korbo, L., Pakkenberg, B., Ladefoged, O., Gundersen, H. J., Arlien-Soborg, P., and Pakkenberg, H. (1990). An efficient method for estimating the total number of neurons in rat brain cortex. J. Neurosci. Methods 31, 93-100. doi: 10.1016/0165-0270(90)90153-7
35. Krutzen, M., Mann, J., Heithaus, M. R., Connor, R. C., Bejder, L., and Sherwin, W. B. (2005). Cultural transmission of tool use in bottlenose dolphins. Proc. Natl. Acad. Sci. U.S.A. 102, 8939-8943. doi: 10.1073/pnas.0500232102
36. Ladygina, N. M., Mass, A. M., and Supin, A. Y. (1978). Multiple sensory projections in the dolphin cerebral cortex. Zh. Vyssh. Nerv. Deiat. 28, 47-1054.
37. Lilly, J. C. (1965). Vocal mimicry in tursiops: ability to match numbers and durations of human vocal bursts. Science 147, 300-301. doi: 10.1126/science.147.3655.300
38. Lilly, J. C., and Miller, A. M. (1961). Vocal exchanges between dolphins: bottlenose dolphins “talk” to each other with whistles, clicks, and a variety of other noises. Science 134, 1873-1876. doi: 10.1126/science.134.3493.1873
39. Lyamin, O. I., Mukhametov, L. M., Siegel, J. M., Nazarenko, E. A., Polyakova, I. G., and Shpak, O. V. (2002). Unihemispheric slow wave sleep and the state of the eyes in a white whale. Behav. Brain Res. 129, 125-129. doi: 10.1016/S0166-4328(01)00346-1
40. Manger, P. R. (2006). An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol. Rev. Camb. Philos. Soc. 81, 293-338. doi: 10.1017/S1464793106007019
41. Manger, P. R. (2013). Questioning the interpretations of behavioral observations of cetaceans: is there really support for a special intellectual status for this mammalian order? Neuroscience 250, 664-696. doi: 10.1016/j.neuroscience.2013.07.041
42. Manger, P. R., Prowse, M., Haagensen, M., and Hemingway, J. (2012). Quantitative analysis of neocortical gyrencephaly in African elephants (Loxodonta africana) and six species of cetaceans: comparison with other mammals. J. Comp. Neurol. 520, 2430-2439. doi: 10.1002/cne.23046
43. Marino, L. (2002). Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav. Evol. 59, 21-32. doi: 10.1159/000063731
44. Marino, L. (2004). Dolphin cognition. Curr. Biol. 14, R910-R911. doi: 10.1016/j.cub.2004.10.010
45. Marino, L. (2008). “Brain evolution,” in Encyclopedia of Marine Mammals, eds W. F. Perrin, B. Würsig, and J. G. M. Thewissen (San Diego, CA: Academic Press), 149-152.
46. Marino, L., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, P. R., Lefebvre, L., et al. (2007). Cetaceans have complex brains for complex cognition. PLoS Biol. 5:e139. doi: 10.1371/journal.pbio.0050139
47. Martin, A. R., and Rothery, P. (1993). Reproductive parameters of female longfinned pilot whales (Globicephala melas) around the Faroe Islands. Rep. Int. Whal. Commn. (Special Issue 14), 263-304.
48. Morgane, P. J., and Glezer, I. I. (1990). “Sensory neocortex in dolphin brain,” in Sensory Abilities of Cetaceans. Laboratory and Field Evidence, eds J. A. Thomas and R. A. Kastelein (New York, NY: Plenum Press), 101-137.
49. Morgane, P. J., Jacobs, M. S., and Mcfarland, W. L. (1980). The anatomy of the brain of the bottlenose dolphin (Tursiops truncates): surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observation sin four other cetacean species. Brain Res. Bull. 5, 1-107. doi: 10.1016/0361-9230(80)90272-5
50. Morgane, P. J., Mcfarland, W. L., and Jacobs, M. S. (1982). The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. J. Hirnforsch. 23, 465-552.
51. Mukhametov, L. M. (1987). Unihemispheric slow-wave sleep in the Amazonian dolphin, Inia geoffrensis. Neurosci. Lett. 79, 128-132. doi: 10.1016/0304-3940(87)90684-7
52. Mukhametov, L. M., Oleksenko, A. I., and Poliakova, I.G. (1988). Quantitative characteristics of the electrocorticographic sleep stages in bottle-nosed dolphins. Neirofiziologiia 20, 532-538.
53. Mundinger, P. C. (1980). Animal cultures and a general theory of cultural evolution. Ethol. Sociobiol. 1, 183-223. doi: 10.1016/0162-3095(80)90008-4
54. Oelschläger, H. A., and Oelschläger, J. S. (2009). “Brain,” in Encyclopedia of Marine Mammals, eds W. F. Perrin, B. Würsig, and J. G. M. Thewissen (San Diego, CA: Academic Press), 134-149.
55. Oelschläger, H. H. A., and Oelschläger, J. S. (2002). “Brain,” in Encyclopedia of Marine Mammals, eds W. F. Perrin, B. Würsig, and J. G. M. Thewissen (San Diego, CA: Academic Press), 133-158.
56. Ottensmeyer, C. A., and Whitehead, H. (2003). Behavioural evidence for social units in long-finned pilot whales. Can. J. Zool. 81, 1327-1338. doi: 10.1139/z03-127
57. Pacini, A. F., Nachtigall, P. E., Kloepper, L. N., Linnenschmidt, M., Sogorb, A., and Matias, S. (2010). Audiogram of a formerly stranded long-finned pilot whale (Globicephala melas) measured using auditory evoked potentials. J. Exp. Biol. 213, 3138-3143. doi: 10.1242/jeb.044636
58. Pakkenberg, B., and Gundersen, H. J. (1997). Neocortical neuron number in humans: effect of sex and age. J. Comp. Neurol. 384, 312-320.
59. Patzke, N., Spocter, M. A., Karlsson, K. A., Bertelsen, M. F., Haagensen, M., Chawana, R., et al. (2013). In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct. Funct. doi: 10.1007/s00429-013-0660-1.[Epub ahead of print].
60. Payne, R. S., and Mcvay (1971). Songs of humpback whales. Science 173, 585-597. doi: 10.1126/science.173.3997.585
61. Plotnik, J. M., De Waal, F. B., and Reiss, D. (2006). Self-recognition in an Asian elephant. Proc. Natl. Acad. Sci. U.S.A. 103, 17053-17057. doi: 10.1073/pnas.0608062103
62. Poth, C., Fung, C., Gunturkun, O., Ridgway, S. H., and Oelschlager, H. H. (2005). Neuron numbers in sensory cortices of five delphinids compared to a physeterid, the pygmy sperm whale. Brain Res. Bull. 66, 357-360. doi: 10.1016/j.brainresbull.2005.02.001
63. Prior, H., Schwarz, A., and Gunturkun, O. (2008). Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition. PLoS Biol. 6:e202. doi: 10.1371/journal.pbio.0060202
64. Ratner, C., Riise, J., Eriksen, N., and Pakkenberg, B. (2010). A postmortem study of the corpus callosum in the common minke whale (Balaenoptera acutorostrata). Mar. Mamm. Sci. 27, 688-700. doi: 10.1111/j.1748-7692.2010.00432.x
65. Reiner, A., Yamamoto, K., and Karten, H. J. (2005). Organization and evolution of the avian forebrain. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1080-1102. doi: 10.1002/ar.a.20253
66. Reiss, D., and Marino, L. (2001). Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc. Natl. Acad. Sci. U.S.A. 98, 5937-5942. doi: 10.1073/pnas.101086398
67. Rendell, L., and Whitehead, H. (2001). Culture in whales and dolphins. Behav. Brain Sci. 24, 309-324. discussion: 324-382. doi: 10.1017/S0140525X0100396X
68. Rice, D. W. (1998). Marine Mammals of the World. Systematics and Distribution. Lawrence, KS: Society for Marine Mammalogy; Allen Press.
69. Ridgway, S. H., and Au, W. W. L. (1999). “Hearing and echolocation: dolphin,” in Elsevier’s Encyclopedia of Neuroscience, eds G. Adelmann and B. H. Smith (New York, NY: Elsevier Science BV), 858-862.
70. Ridgway, S., Houser, D., Finneran, J., Carder, D., Keogh, M., Van Bonn, W., et al. (2006). Functional imaging of dolphin brain metabolism and blood flow. J. Exp. Biol. 209, 2902-2910. doi: 10.1242/jeb.02348
71. Roth, G., and Dicke, U. (2005). Evolution of the brain and intelligence. Trends Cogn. Sci. 9, 250-257. doi: 10.1016/j.tics.2005.03.005
72. Sherwood, C. C., Stimpson, C. D., Raghanti, M. A., Wildman, D. E., Uddin, M., Grossman, L. I., et al. (2006). Evolution of increased glia-neuron ratios in the human frontal cortex. Proc. Natl. Acad. Sci. U.S.A. 103, 13606-13611. doi: 10.1073/pnas.0605843103
73. Supin, A. Y., Mukhametov, L. M., Ladygina, T. F., Popov, V. V., Mass, A. M., and Polyakova, I. G. (1978). Electrophysiological Studies of the Dolphin’s Brain (in Russia). (Moscow: Izdatel’stvo Nauka), 7-85.
74. Tarpley, R. J., and Ridgway, S. H. (1994). Corpus callosum size in delphinid cetaceans. Brain Behav. Evol. 44, 156-165. doi: 10.1159/000113587
75. Teilmann, J., Larsen, F., and Desportes, G. (2007). Time allocation and diving behaviour of harbour porpoises (Phocoena phocoena) in Danish and adjacent waters. J. Cetacean Res. Man. 9, 201-210.
76. Waller, G. N. H. (1992). Ciliary mucscles in the eye of the long-finned pilot whale Globicephala melaena (Traill, 1809). Aquat. Mamm. 18, 36-39.
77. Walloe, S., Eriksen, N., Dabelsteen, T., and Pakkenberg, B. (2010). A neurological comparative study of the harp seal (Pagophilus groenlandicus) and harbor porpoise (Phocoena phocoena) brain. Anat. Rec. (Hoboken) 293, 2129-2135. doi: 10.1002/ar.21295
78. West, M. J., Slomianka, L., and Gundersen, H. J. (1991). Unbiased stereolog- ical estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482-497. doi: 10.1002/ar.1092310411
79. Williams, R. W., and Herrup, K. (1988). The control of neuron number. Annu. Rev. Neurosci. 11, 423-453. doi: 10.1146/annurev.ne.11.030188.002231
80. Wong, P., Peebles, J. K., Asplund, C. L., Collins, C. E., Herculano-Houzel, S., and Kaas, J. H. (2013). Faster scaling of auditory neurons in cortical areas relative to subcortical structures in primate brains. Brain Behav. Evol. 81, 209-218. doi: 10.1159/000350709