Topographical and structural characterization of the V1-V2 transition zone in the visual cortex of the long-finned pilot whale Globicephala melas (Traill, 1809).

calretinin cetaceans cetartiodactyla cytoarchitecture dolphin globicephala visual cortex whale

Journal

Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775

Informations de publication

Date de publication:
05 2021
Historique:
revised: 11 09 2020
received: 31 07 2020
accepted: 06 10 2020
pubmed: 30 10 2020
medline: 14 7 2021
entrez: 29 10 2020
Statut: ppublish

Résumé

The visual system of cetaceans is at best poorly understood. With a handful of electrophysiological studies and a limited number of histological preparations from well-preserved specimen, the investigation of the principles underlying the cortical organization in cetaceans remains a challenge. In the course of our current investigation, we identified the transition from V2 to V1 in the long-finned pilot whale Globicephala melas, only recognizable through immunocytochemistry, and a similar if not homologue transition in the sheep Ovis aries. Our results emphasize the importance of differential pattern recognition in which the application of different markers uncovers a diversity in a delphinid's cortex, formerly widely considered as uniform and archetypal. In fact, the evidence that we present suggests the existence of relatively unacknowledged areas beyond the well-known sensory territories in cetaceans.

Identifiants

pubmed: 33119932
doi: 10.1002/ar.24558
doi:

Substances chimiques

Calbindin 2 0
Calbindins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1105-1118

Informations de copyright

© 2021 American Association for Anatomy.

Références

Berns, G. S., Cook, P. F., Foxley, S., Jbabdi, S., Miller, K. L., & Marino, L. (2015). Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe. Proceedings of the Royal Society B: Biological Sciences, 282, 20151203. https://doi.org/10.1098/rspb.2015.1203
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Großhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Berlin: J.A. Barth.
Bullock, T. H., & Ridgway, S. H. (1972). Evoked potentials in the central auditory system of alert porpoises to their own and artificial sounds. Journal of Neurobiology, 3, 79-99. https://doi.org/10.1007/978-1-4684-9427-3_35
Bullock, T. H., Grinnell, A. D., Ikezono, E., Kameda, K., Katsuki, Y., Nomoto, M., … Yanagisawa, K. (1968). Electrophysiological studies of central auditory mechanisms in cetaceans. Zeitschrift für Vergleichende Physiologie, 59, 117-156. https://doi.org/10.1007/BF00339347
Camp, A. J., & Wijesinghe, R. (2009). Calretinin: Modulator of neuronal excitability. The International Journal of Biochemistry & Cell Biology, 41, 2118-2121. https://doi.org/10.1016/j.biocel.2009.05.007
Clarke, P. G. H., Donaldson, I. M., & Whitteridge, D. (1976). Binocular visual mechanisms in cortical areas I and II of the sheep. The Journal of Physiology, 256, 509-526. https://doi.org/10.1113/jphysiol.1976.sp011336
Clarke, P. G. H., & Whitteridge, D. (1976). The cortical visual areas of the sheep. The Journal of Physiology, 256, 497-508. https://doi.org/10.1113/jphysiol.1976.sp011335
Cozzi, B., Huggenberger, S., & Oelschläger, H. A. (2017). Anatomy of dolphins (1st ed.), Amsterdam: Academic Press.
Cozzi, B., Roncon, G., Granato, A., Giurisato, M., Castagna, M., Peruffo, A., … Pirone, A. (2014). The claustrum of the bottlenose dolphin Tursiops truncatus (Montagu 1821). Frontiers in Systems Neuroscience, 8, 42. https://doi.org/10.3389/fnsys.2014.00042
DeFelipe, J. (1997). Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin- D28k, parvalbumin and calretinin in the neocortex. Journal of Chemical Neuroanatomy, 14, 1-19.
Defelipe, J., González-Albo, M. C., Del Río, M. R., & Elston, G. N. (1999). Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. The Journal of Comparative Neurology, 412, 515-526. https://doi.org/10.1002/(SICI)1096-9861(19990927)412:3<515::AID-CNE10>3.0.CO;2-1
DeFelipe, J., Hendry, S. H. C., & Jones, E. G. (1986). A correlative electron microscopic study of basket cells and large gabaergic neurons in the monkey sensory-motor cortex. Neuroscience, 17, 991-1009. https://doi.org/10.1016/0306-4522(86)90075-8
DeFelipe, J., Hendry, S. H. C., & Jones, E. G. (1989a). Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Research, 503, 49-54. https://doi.org/10.1016/0006-8993(89)91702-2
Defelipe, J., Hendry, S. H. C., Jones, E. G., & Schmechel, D. (1985). Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. The Journal of Comparative Neurology, 231, 364-384. https://doi.org/10.1002/cne.902310307
DeFelipe, J., Hendry, S. H., & Jones, E. G. (1989b). Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proceedings of the National Academy of Sciences, 86, 2093-2097. https://doi.org/10.1073/pnas.86.6.2093
DeFelipe, J., & Jones, E. (1985). Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. The Journal of Neuroscience, 5, 3246-3260. https://doi.org/10.1523/JNEUROSCI.05-12-03246.1985
Fitzpatrick, D., Lund, J. S., Schmechel, D. E., & Towles, A. C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. The Journal of Comparative Neurology, 264, 73-91. https://doi.org/10.1002/cne.902640107
Garey, L. J., & 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. The Journal of Comparative Neurology, 247, 491-496. https://doi.org/10.1002/cne.902470408
Garey, L. J., & Revishchin, A. V. (1988). Laminar distribution of cytochrome oxidase activity in the porpoise neocortex. Doklady Akademii Nauk SSSR, 302, 1486-1489.
Garey, L. J., & Revishchin, A. V. (1990). Structure and Thalamocortical relations of the cetacean sensory cortex: Histological, tracer and Immunocytochemical studies. In J. Thomas & R. A. Kastelein (Eds.), Sensory Abilities of Cetaceans (pp. 19-30). Boston, MA: Springer US.
Garey, L. J., Takács, J., Revishchin, A. V., & Hámori, J. (1989). Quantitative distribution of GABA-immunoreactive neurons in cetacean visual cortex is similar to that in land mammals. Brain Research, 485, 278-284. https://doi.org/10.1016/0006-8993(89)90571-4
Garey, L. J., Winkelmann, E., & Brauer, K. (1985). Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. The Journal of Comparative Neurology, 240, 305-321. https://doi.org/10.1002/cne.902400307
Glezer, I. I., Hof, P. R., Istomin, V. V., & Morgane, P. J. (1995). Comparative immunocytochemistry of calcium-binding protein-positive neurons in visual and auditory systems of cetacean and primate brains. In R. A. Kastelein, J. A. Thomas, & P. E. Nachtigall (Eds.), Sensory systems of aquatic mammals (pp. 477-513). The Netherlands: De Spil Publishers, Woerden.
Glezer, I. I., Hof, P. R., Leranth, C., & Morgane, P. J. (1992a). Morphological and histochemical features of odontocete visual neocortex: Immunocytochemical analysis of pyramidal and nonpyramidal populations of neurons. In J. A. Thomas, R. A. Kastelein, & A. Y. Supin (Eds.), Marine mammal sensory systems (pp. 1-38). New York: Plenum Press.
Glezer, I. I., Hof, P. R., Leranth, C., & Morgane, P. J. (1993). Calcium-binding protein-containing neuronal populations in mammalian visual cortex: A comparative study in whales, insectivores, bats, rodents, and primates. Cerebral Cortex, 3, 249-272. https://doi.org/10.1093/cercor/3.3.249
Glezer, I. I., Hof, P. R., & Morgane, P. J. (1992b). Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Research, 595, 181-188. https://doi.org/10.1016/0006-8993(92)91047-I
Glezer, I. I., Hof, P. R., & Morgane, P. J. (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). Journal of Chemical Neuroanatomy, 15, 203-237. https://doi.org/10.1016/S0891-0618(98)00022-2
Glezer, I. I., Jacobs, M. S., & Morgane, P. J. (1988). Implications of the “initial brain” concept for brain evolution in Cetacea. The Behavioral and Brain Sciences, 11, 75-89. https://doi.org/10.1017/S0140525X0005281X
Glezer, I. I., & 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 Research Bulletin, 24, 401-427. https://doi.org/10.1016/0361-9230(90)90096-I
Glezer, I. I., Morgane, P. J., & Leranth, C. (1990). Immunocytochemistry of neurotransmitters in visual Neocortex of several toothed whales: Light and electron microscopic study. In Sensory abilities of cetaceans (pp. 39-66). Boston, MA: Springer US. https://doi.org/10.1007/978-1-4899-0858-2_4
Goebel, R., Muckli, L., & Kim, D.-S. (2012). Visual System. In T. H. N. System (Ed.), J. K. Mai and G. Paxinos (pp. 1301-1327). Amsterdam: Elsevier Academic Press.
Goldman-Rakic, P. S., & Schwartz, M. L. (1982). Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Science, 216(4547), 755-757.
Graïc, J.-M., Peruffo, A., Ballarin, C., & Cozzi, B. (2017). The brain of the giraffe (Giraffa camelopardalis): Surface configuration, Encephalization quotient, and analysis of the existing literature. The Anatomical Record, 300(8), 1502-1511. https://doi.org/10.1002/ar.23593
Graïc, J.-M., Corain, L., Peruffo, A., Cozzi, B., & Swaab, D. F. (2018). The bovine anterior hypothalamus: Characterization of the vasopressin-oxytocin containing nucleus and changes in relation to sexual differentiation. Journal of Comparative Neurology, 526(17), 2898-2917. https://doi.org/10.1002/cne.24542
Hendry, S. H. C., Jones, E. G., Emson, P. C., Lawson, D. E. M., Heizmann, C. W., & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Experimental Brain Research, 76, 467-472. https://doi.org/10.1007/BF00247904
Herman, L. M., & Pack, A. A. (1992). Echoic-visual cross-modal recognition by a dolphin. In Marine mammal sensory systems (pp. 709-726). Boston, MA: Springer US.
Herman, L. M., Pack, A. A., & Hoffmann-Kuhnt, M. (1998). Seeing through sound: Dolphins (Tursiops truncatus) perceive the spatial structure of objects through echolocation. Journal of Comparative Psychology, 112, 292-305. https://doi.org/10.1037/0735-7036.112.3.292
Hof, P. R., Cox, K., Young, W. G., Celio, M. R., Rogers, J., & Morrison, J. H. (1991). Parvalbumin-lmmunoreactive neurons in the Neocortex are resistant to degeneration in Alzheimerʼs disease. Journal of Neuropathology and Experimental Neurology, 50, 451-462. https://doi.org/10.1097/00005072-199107000-00006
Hof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., & Vogt Weisenhorn, D. M. (1999). Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. Journal of Chemical Neuroanatomy, 16, 77-116. https://doi.org/10.1016/S0891-0618(98)00065-9
Hof, P. R., & Morrison, J. H. (1991). Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer’s disease. Experimental Neurology, 111, 293-301. https://doi.org/10.1016/0014-4886(91)90096-U
Howard, I. P., & Rogers, B. J. (1996). The physiology of binocular vision. In I. P. Howard & B. J. Rogers (Eds.), Binocular vision and stereopsis (pp. 105-148). New York: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780195084764.003.0004
Huggenberger, S., Oelschläger, H. H. A., & Cozzi, B. (2019). Atlas of the anatomy of dolphins and whales, Amsterdam: Academic Press.
John, S. E., Lovell, T. J. H., Opie, N. L., Wilson, S., Scordas, T. C., Wong, Y. T., … Oxley, T. J. (2017). The ovine motor cortex: A review of functional mapping and cytoarchitecture. Neuroscience and Biobehavioral Reviews, 80, 306-315. https://doi.org/10.1016/j.neubiorev.2017.06.002
Karamanlidis, A. N., Saigal, R. P., Giolli, R. A., Mangana, O., & Michaloudi, H. (1979). Visual thalamocortical connections in sheep studied by means of the retrograde transport of horseradish-peroxidase. The Journal of Comparative Neurology, 187, 245-259. https://doi.org/10.1002/cne.901870202
Kern, A., Siebert, U., Cozzi, B., Hof, P. R., & Oelschläger, H. A. (2011). Stereology of the neocortex in odontocetes: Qualitative, quantitative, and functional implications. Brain, Behavior and Evolution, 77, 79-90. https://doi.org/10.1159/000323674
Kesarev, V. (1971). The inferior brain of the dolphin. Soviet Science Review, 1, 52-58.
Kesarev, V. S. (1969). Structural organization of the limbic cortex in dolphins. Neuroscience Translations, 3, 40-46. https://doi.org/10.1007/BF01124284
Kesarev, V. S., & Malofeeva, L. I. (1969). Structural organization of the dolphin motor cortex. Neuroscience Translations, 3, 33-39. https://doi.org/10.1007/BF01124283
Kesarev, V. S., Malofeeva, L. I., & Trykova, O. V. (1977). Structural organization of the cetacean neocortex. Arkhiv Anatomii, Gistologii i Émbriologii, 73, 23-30.
Kosaka, T., Heizmann, C. W., Tateishi, K., Hamaoka, Y., & Hama, K. (1987). An aspect of the organizational principle of the γ-aminobutyric acidergic system in the cerebral cortex. Brain Research, 409, 403-408. https://doi.org/10.1016/0006-8993(87)90732-3
Ladygina, T. F., Mass, A. M., & Supin, A. I. (1978). Multiple sensory projections in the dolphin cerebral cortex. Zhurnal Vyssheĭ Nervnoĭ Deiatelnosti Imeni I P Pavlova, 28, 1047-1053.
Ladygina, T. F., & Supin, A. I. (1977). Localization of the sensory projection areas in the cerebral cortex of the dolphin, Tursiops truncatus. Zhurnal Evoliutsionnoĭ Biokhimii i Fiziologii, 13, 712-718.
Ladygina, T. F., & Supin, A. Y. (1970). Acoustic projection in the dolphin cerebral cortex. Fiziologicheskiĭ Zhurnal SSSR Imeni I. M. Sechenova, 56, 1554-1560.
Lende, R. A., & Akdikmen, S. (1968). Motor field in cerebral cortex of the bottlenose dolphin. Journal of Neurosurgery, 29, 495-499. https://doi.org/10.3171/jns.1968.29.5.0495
Lende, R. A., & Welker, W. I. (1972). An unusual sensory area in the cerebral neocortex of the bottlenose dolphin, Tursiops truncatus. Brain Research, 45, 555-560. https://doi.org/10.1016/0006-8993(72)90482-9
Minervini, S., Accogli, G., Pirone, A., Graïc, J.-M., Cozzi, B., & Desantis, S. (2016). Brain mass and encephalization quotients in the domestic industrial pig (Sus scrofa). PLoS One, 11(6), e0157378. https://doi.org/10.1371/journal.pone.0157378
Morgane, P. J., and Glezer, I. I. (1990). “Sensory Neocortex in Dolphin Brain,” in Sensory Abilities of Cetaceans, eds. J. A. Thomas and R. A. Kastelein (NATO ASI Series and Plenum Science Publishing), 107-136.
Morgane, P. J., Glezer, I. I., & Jacobs, M. S. (1988). Visual cortex of the dolphin: An image analysis study. The Journal of Comparative Neurology, 273, 3-25. https://doi.org/10.1002/cne.902730103
Morgane, P. J., Glezer, I. I., and Jacobs, M. S. (1990). “Comparative and evolutionary anatomy of the visual cortex of the dolphin,” in E. G. Jones and A. Peters (Eds.), Cerebral Cortex (Vol. 8B, pp. 215-262), New York: Plenum Press.
Morgane, P. J., & Jacobs, M. S. (1972). Comparative anatomy of the cetacean nervous System. In Functional anatomy of marine mammals (Vol. 1, pp. 117-244). London: Academic Press.
Morgane, P. J., Jacobs, M. S., & Galaburda, A. M. (1986). Evolutionary morphology of the dolphin brain. In R. J. Schusterman, J. A. Thomas, & F. G. Wood (Eds.), Dolphin cognition and behavior: A comparative approach (pp. 5-28). Hillsdale, NJ: Lawrence Erlbaum Associates, Inc.
Morgane, P. J., Jacobs, M. S., & McFarland, W. L. (1980). The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetacean species. Brain Research Bulletin, 5, 1-107. https://doi.org/10.1016/0361-9230(80)90272-5
Mortensen, H. S., Pakkenberg, B., Dam, M., Dietz, R., Sonne, C., Mikkelsen, B., & Eriksen, N. (2014). Quantitative relationships in delphinid neocortex. Frontiers in Neuroanatomy, 8, 1-10. https://doi.org/10.3389/fnana.2014.00132
Mukhametov, L. M., Supin, A. Y., & Polyakova, I. G. (1977). Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins. Brain Research, 134, 581-584. https://doi.org/10.1016/0006-8993(77)90835-6
Pack, A. A., & Herman, L. M. (1995). Sensory integration in the bottlenosed dolphin: Immediate recognition of complex shapes across the senses of echolocation and vision. The Journal of the Acoustical Society of America, 98, 722-733. https://doi.org/10.1121/1.413566
Peruffo, A., Corain, L., Bombardi, C., Centelleghe, C., Grisan, E., Graïc, J.-M., … Cozzi, B. (2019). The motor cortex of the sheep: Laminar organization, projections and diffusion tensor imaging of the intracranial pyramidal and extrapyramidal tracts. Brain Structure & Function, 224, 1933-1946. https://doi.org/10.1007/s00429-019-01885-x
Popov, V. V., Ladygina, T. F., & Supin, A. Y. (1986). Evoked potentials of the auditory cortex of the porpoise, Phocoena phocoena. Journal of Comparative Physiology A, 158, 705-711. https://doi.org/10.1007/BF00603828
Popov, V. V., & Supin, A. Y. (2007). Analysis of auditory information in the brains of cetaceans. Neuroscience and Behavioral Physiology, 37, 285-291. https://doi.org/10.1007/s11055-007-0013-8
Revishchin, A. V., & Garey, L. J. (1990). The thalamic projection to the sensory neocortex of the porpoise, Phocoena phocoena. Journal of Anatomy, 169, 85-102.
Richard, P. (1967). Atlas stéréotaxique du cerveau de Brebis “Préalpes-du-Sud”. Paris, France: Institut National de la Recherche Agronomique.
Ridgway, S. H. (1986). Physiological observations on dolphin brains. In R. J. Schusterman J. A. Thomas & F. G. Woods (Eds.), Dolphin cognition and behavior: A comparative approach. (pp. 31-59). Hillsdale, NJ: Lawrence Erlbaum Associates, Inc.
Rogers, J. H. (1987). Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons. The Journal of Cell Biology, 105, 1343-1353. https://doi.org/10.1083/jcb.105.3.1343
Rose, J. E. (1942). A cytoarchitectural study of the sheep cortex. The Journal of Comparative Neurology, 76, 1-55. https://doi.org/10.1002/cne.900760102
Serafetinides, E. A., Shurley, J. T., & Brooks, R. E. (1971). Electroencephalogram of the pilot whale globicephala scammoni, in wakefullness and sleep: Lateralization aspects. International Journal of Psychobiology, 2, 123-135.
Shurley, J. T., Serafetinides, E. A., Brooks, R. E., Elsner, R., & Kenney, D. W. (1969). Sleep in cetaceans. I. the pilot whale, Globicephala scammoni. Psychophysiology, 6, 230.
Sokolov, V. E., Ladygina, T. F., & Supin, A. I. (1972). Localization of sensory zones in the dolphin cerebral cortex. Doklady Akademii Nauk SSSR, 202, 490-493.
Supin, A. Y., Mukhametov, L. M., Ladygina, T. F., Popov, V. V., Mass, A. M., & Polyakova, I. (1978). Electrophysiological studies of the dolphin’s brain (in Russ.). Moscow: Izd. Nauka.
Supin, A. Y., Popov, V. V., & Mass, A. M. (2001). The sensory physiology of aquatic mammals. Boston, MA: Springer US. https://doi.org/10.1007/978-1-4615-1647-7
Van Kann, E., Cozzi, B., Hof, P. R., & Oelschläger, H. A. (2017). Qualitative and quantitative analysis of primary neocortical areas in selected mammals. Brain, Behavior and Evolution, 90, 193-210. https://doi.org/10.1159/000477431
Vanderwolf, C. H., & Cooley, R. K. (2002). The sheep brain: A photographic Series (2nd ed.). London, Ontario: A. J. Kirby Co.
Wright, A., Scadeng, M., Stec, D., Dubowitz, R., Ridgway, S., & Leger, J. S. (2017). Neuroanatomy of the killer whale (Orcinus orca): A magnetic resonance imaging investigation of structure with insights on function and evolution. Brain Structure & Function, 222, 417-436. https://doi.org/10.1007/s00429-016-1225-x
Zilles, K., & Palomero-Gallagher, N. (2017). Comparative analysis of receptor types that identify primary cortical sensory areas. In J. H. Kaas (Ed.), Evolution of nervous systems (2nd ed., pp. 225-245). Amsterdam: Academic Press.

Auteurs

Jean-Marie Graïc (JM)

Department of Comparative Biomedicine and Food Science, University of Padova, Legnaro (PD), Italy.

Antonella Peruffo (A)

Department of Comparative Biomedicine and Food Science, University of Padova, Legnaro (PD), Italy.

Annamaria Grandis (A)

Department of Veterinary Medical Sciences, University of Bologna, Ozzano dell'Emilia (BO), Italy.

Bruno Cozzi (B)

Department of Comparative Biomedicine and Food Science, University of Padova, Legnaro (PD), Italy.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH