The neurobiology of Etruscan shrew active touch

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1581, 2011, Pages 3026-3036

  Brecht, Michael ^a   Naumann, Robert ^a   Anjum, Farzana ^a   Wolfe, Jason ^a   Munz, Martin ^a   Mende, Carolin ^a   Roth Alpermann, Claudia ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Active touch; Barrel cortex; Shrew; Suncus etruscus; Vibrissa; Whisker

Indexed keywords

BODY SIZE; BODY TEMPERATURE; CRICKET; ENDOTHERMY; EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; HAIR; MECHANORECEPTION; METABOLISM; MORTALITY; MOVEMENT; MUSCLE; NEUROLOGY; PSYCHOLOGY; SENSORY SYSTEM; SMALL MAMMAL; STEROID;

ANIMALIA; HEXAPODA; MAMMALIA; SORICIDAE; SUNCUS ETRUSCUS;

EID: 80053505353     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0160     Document Type: Review

References (82)

1. Nelson, M. E. & MacIver, M. A. 2006 Sensory acquisition in active sensing systems. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 192, 573-586. (doi:10.1007/s00359-006-0099-4)
2. Spitzenberger, F. 1990 Suncus etruscus (Savi, 1822)-Etruskerspitzmaus. In Handbuch der Säugetiere Europas:-Bd (eds J. Niethammer & F. Krapp), pp. 375-392. Wiesbaden: Aula Verlag.
3. Tauber, E. & Camhi, J. 1995 The wind-evoked escape behavior of the cricket Gryllus bimaculatus: integration of behavioral elements. J. Exp. Biol. 198, 1895-1907.
4. Jürgens, K. D., Fons, R., Peters, T. & Sender, S. 1996 Heart and respiratory rates and their significance for convective oxygen transport rates in the smallest mammal, the Etruscan shrew Suncus etruscus. J. Exp. Biol. 199, 2579-2584.
5. Catania, K. C. 2000 Epidermal sensory organs of moles, shrew moles, and desmans: a study of the family Talpidae with comments on the function and evolution of Eimer's organ. Brain Behav. Evol. 56, 146-174. (doi:10.1159/000047201)
6. Anjum, F., Turni, H., Mulder, P. G. H., van der Burg, J. & Brecht, M. 2006 Tactile guidance of prey capture in Etruscan shrews. Proc. Natl Acad. Sci. USA 103, 16 544-16 549. (doi:10.1073/pnas.0605573103)
7. Munz, M., Brecht, M. & Wolfe, J. 2010 Active touch during shrew prey capture. Front. Behav. Neurosci. 4, 191. (doi:10.3389/fnbeh.2010.00191)
8. Grünwald, A. 1969 Untersuchungen zur Orientierung der Weisszahnspitzmäuse (Soricidae-Crocidurinae). Z. Vergl. Physiol. 65, 191-217. (doi:10.1007/BF00297683)
9. Churchfield, S. 1990 The natural history of shrews. CA, USA: Comstock.
10. Stephan, H., Baron, G. & Frahm, H. D. 1991 Insectivora: with a stereotaxic atlas of the hedgehog brain. Berlin, Germany: Springer.
11. Merriam, C. 1884 Blarina brevicauda. The mammals of the Adirnondack region, northeastern New York. New York, NY: L. S. Foster Press.
12. Seton, E. T. 1909 Life-histories of northern animals: an account of the mammals of Manitoba/by Ernest Thompson Seton, naturalist to the Government of Manitoba; with 68 maps and 560 drawings by the author. New York, NY: Scribner. See http://www.biodiversitylibrary.org/bibliography/8824.
13. Branis, M. & Burda, H. 1994 Visual and hearing biology of shrews. In Advances in the biology of shrews (eds J. F. Merritt, G. L. Kirkland & R. K. Rose), pp. 189-200. Pittsburgh, PA: Carnegie Museum of Natural History Press.
14. Burda, H. 1979 Morphology of the middle and inner ear in some species of shrews (Insectivora, Soricidae). Acta Sci. Nat. Brno 13, 1-48.
15. Catania, K. C., Lyon, D. C., Mock, O. B. & Kaas, J.H. 1999 Cortical organization in shrews: evidence from five species. J. Comp. Neurol. 410, 55-72. (doi:10.1002/(SICI)1096-9861(19990719)410:1,55::AID-CNE6.3.0.CO;2-2)
16. Roth-Alpermann, C., Anjum, F., Naumann, R. & Brecht, M. 2010 Cortical organization in the Etruscan shrew (Suncus etruscus). J. Neurophysiol. 104, 2389-2406. (doi:10.1152/jn.00762.2009)
17. Schmidt, U. 1979 Die Lokalisation vergrabenen Futters bei der Hausspitzmaus Crocidura russula Hermann. Z. f. Säugetierkunde 44, 59-60.
18. Schmidt, U. & Nadolski, A. 1979 Die Verteilung von olfaktorischem und respiratorischem Epithel in der Nasenhöhle der Hausspitzmaus, Crocidura russula Hermann. Z. f. Säugetierkunde 44, 18-25.
19. Catania, K. C., Hare, J. F. & Campbell, K. L. 2008 Water shrews detect movement, shape, and smell to find prey underwater. Proc. Natl Acad. Sci. USA 105, 571-576. (doi:10.1073/pnas.0709534104)
20. Niven, J. E. & Laughlin, S. B. 2008 Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211, 1792-1804. (doi:10.1242/jeb.017574)
21. Catania, K. C. 2005 Evolution of sensory specializations in insectivores. Anat. Rec. Discov. Mol. Cell Evol. Biol. 287, 1038-1050. (doi:10.1002/ar.a.20265)
22. Crish, S. D., Rice, F. L., Park, T. J. & Comer, C. M. 2003 Somatosensory organization and behavior in naked mole-rats I: vibrissa-like body hairs comprise a sensory array that mediates orientation to tactile stimuli. Brain Behav. Evol. 62, 141-151. (doi:10.1159/000072723)
23. Hetling, J. R., Baig-Silva, M. S., Comer, C.M., Pardue, M. T., Samaan, D. Y., Qtaishat, N. M., Pepperberg, D. R. & Park, T. J. 2005 Features of visual function in the naked mole-rat Heterocephalus glaber. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 317-330. (doi:10.1007/s00359-004-0584-6)
24. Frey, H. 1979 La température corporelle de Suncus etruscus (Soricidae, Insectivora) au cours de l'activité, du repos normothermique et de la torpeur. Rev. Suisse Zool. 86, 653-662.
25. Ishii, K., Uchino, M., Kuwahara, M., Tsubone, H. & Ebukuro, S. 2002 Diurnal fluctuations of heart rate, body temperature and locomotor activity in the house musk shrew (Suncus murinus). Exp. Anim. 51, 57-62. (doi:10.1538/expanim.51.57)
26. Frey, H. & Vogel, P. 1979 Etude de la torpeur chez Suncus etruscus (Savi, 1822) (Soricidae, Insectivora) en captivite. Rev. Suisse Zool. 81, 23-36.
27. Fons, R., Sender, S., Peters, T. & Jürgens, K. D. 1997 Rates of rewarming, heart and respiratory rates and their significance for oxygen transport during arousal from torpor in the smallest mammal, the Etruscan shrew Suncus etruscus. J. Exp. Biol. 200, 1451-1458.
28. Peters, T., Kubis, H. P., Wetzel, P., Sender, S., Asmussen, G., Fons, R. & Jürgens, K. D. 1999 Contraction parameters, myosin composition and metabolic enzymes of the skeletal muscles of the Etruscan shrew Suncus etruscus and of the common European whitetoothed shrew Crocidura russula (Insectivora: Soricidae). J. Exp. Biol. 202, 2461-2473.
29. Morrison, P., Ryser, F. A. & Dawe, A. R. 1959 Studies on the physiology of the masked shrew Sorex cinereus. Physiol. Zool. 32, 256-271.
30. Jürgens, K. D. 2002 Etruscan shrew muscle: the consequences of being small. J. Exp. Biol. 205, 2161-2166.
31. Fons, R., Stephan, H. & Baron, G. 1984 Brains of Soricidae. I. Encephalization and macromorphology, with special reference to Suncus etruscus. Z. Zool. Syst. Evol.-forsch. 22, 145-158. (doi:10.1111/j.1439-0469.1984.tb00653.x)
32. Wang, S. S., Shultz, J. R., Burish, M. J., Harrison, K. H., Hof, P. R., Towns, L. C., Wagers, M. W. & Wyatt, K. D. 2008 Functional trade-offs in white matter axonal scaling. J. Neurosci. 28, 4047-4056. (doi:10.1523/ JNEUROSCI.5559-05.2008)
33. Kielan-Jaworowska, Z. 2004 Mammals from the age of dinosaurs: origins, evolution, and structure. New York, NY: Columbia University Press.
34. Catania, K. C. & Henry, E. C. 2006 Touching on somatosensory specializations in mammals. Curr. Opin. Neurobiol. 16, 467-473. (doi:10.1016/j.conb.2006.06.010)
35. Vogel, P. 1970 Biologische Betrachtungen an Etruskerspitzmäusen (Suncus etruscus Savi, 1822). Z. f. Säugetierkunde 33, 173-185.
36. Davison, G. 1979 Some notes on Savi's pygmy shrew. Malay. Nat. J. 32, 227-231.
37. Nowak, R. M. 1999 Walker's mammals of the world. Baltimore, MD: JHU Press.
38. Hutterer, R. & Kock, D. 2002 Recent and ancient records of shrews from Syria, with notes on Crocidura katinka Bate, 1937 (Mammalia: Soricidae). Bonner zool. Beitr. 50, 249-258.
39. Churchfield, S. 2002 Why are shrews so small? The costs and benefits of small size in northern temperate Sorex species in the context of foraging habits and prey supply. Acta Theriol. 47, 169-184. (doi:10.1007/ BF03192486)
40. Saint Girons, M. C. 1957 Contribution à la connaissance de la Pachyure étrusque en captivité. Mammalia 21, 69-76. (doi:10.1515/mamm.1957.21.1.69)
41. Geraets, A. 1972 Aktivitätsmuster und Nahrungsbedarf bei Suncus etruscus. Bonn. zool. Beitr. 23, 181-196.
42. Vogel, P. 1974 Kälteresistenz und reversible Hypothermie der Etruskerspitzmaus (Suncus etruscus Soricidae, Insectivora). Z. f. Säugetierkunde 35, 173-185.
43. Halle, S. 2006 Polyphasic activity patterns in small mammals. Folia Primatol. 77, 15-26. (doi:10.1159/000089693)
44. Haberl, W. 1993 Ecology of Austrian shrews in a wetland of the Waldviertel region (Lower Austria) and experimental studies on their behaviour. PhD thesis, University of Vienna.
45. Gould, E., Negus, N. C. & Novick, A. 1964 Evidence for echolocation in shrews. J. Exp. Zool. 156, 19-37. (doi:10.1002/jez.1401560103)
46. Buchler, E. 1976 The use of echolocation by the wandering shrew (Sorex vagrans). Anim. Behav. 24, 858-873. (doi:10.1016/S0003-3472(76)80016-4)
47. Tomasi, T. E. 1979 Echolocation by the short-tailed shrew Blarina brevicauda. J. Mammal. 60, 751-759. (doi:10.2307/1380190).
48. Thomas, J. A. & Jalili, M. S. 2004 Review of echolocation in insectivores and rodents. In Echolocation in bats and dolphins (eds J. A. Thomas, C. F. Moss & M. Vater). Chicago, IL: University of Chicago Press.
49. Siemers, B. M., Schauermann, G., Turni, H. & von Merten, S. 2009 Why do shrews twitter? Communication or simple echo-based orientation. Biol. Lett 5, 593-596. (doi:10.1098/rsbl.2009.0378)
50. von Uexküll, J. 1957 A stroll through the worlds of animals and men: a picture book of invisible worlds. Instinctive behavior: the development of a modern concept (ed. C. H. Schiller), pp. 5-80. New York, NY: International Universities Press.
51. Comer, C. & Yoshichika, B. 2011 Active touch in orthopteroid insects: behaviours, multisensory substrates and evolution. Phil. Trans. R. Soc. B 366, 3006-3015. (doi:10.1098/rstb.2011.0149)
52. Gnatzy, W. & Heusslein, R. 1986 Digger wasp against crickets. Naturwissenschaften 73, 212-215. (doi:10.1007/BF00417728)
53. Gnatzy, W. & Hustert, R. 1989 Mechanoreceptors in behavior. In Cricket behavior and neurobiology (eds F. Huber, T. E. Moore & W. Loher), pp. 198-226. Ithaca, NY: Cornel University Press.
54. Edwards, J. S. & Palka, J. 1974 The cerci and abdominal giant fibres of the house cricket, Acheta domesticus. I. Anatomy and physiology of normal adults. Proc. R. Soc. Lond. B 185, 83-103. (doi:10.1098/rspb.1974.0007)
55. Walthall, W. W. & Murphey, R. K. 1986 Positional information, compartments, and the cercal sensory system of crickets. Dev. Biol. 113, 182-200. (doi:10.1016/0012-1606(86)90121-1)
56. Miller, J. P., Jacobs, G. A. & Theunissen, F. E. 1991 Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons. J. Neurophysiol. 66, 1680-1689.
57. Theunissen, F. E. & Miller, J. P. 1991 Representation of sensory information in the cricket cercal sensory system. II. Information theoretic calculation of system accuracy and optimal tuning-curve widths of four primary interneurons. J. Neurophysiol. 66, 1690-1703.
58. Jacobs, G. A., Miller, J. P. & Aldworth, Z. 2008 Computational mechanisms of mechanosensory processing in the cricket. J. Exp. Biol. 211, 1819-1828. (doi:10.1242/ jeb.016402).
59. Gras, H. & Hörner, M. 1992 Wind-evoked escape running of the cricket Gryllus bimaculatus. I. Behavioural analysis. J. Exp. Biol. 171, 189-214.
60. Baba, Y. & Shimozawa, T. 1997 Diversity of motor responses initiated by a wind stimulus in the freely moving cricket, Gryllus bimaculatus. Zool. Sci. 14, 587-594. (doi:10.2108/zsj.14.587)
61. Hustert, R. & Gnatzy, W. 1995 The motor program for defensive kicking in crickets: performance and neural control. J. Exp. Biol. 198, 1275-1283.
62. Jin, T., Witzemann, V. & Brecht, M. 2004 Fiber types of the intrinsic whisker muscle and whisking behavior. J. Neurosci. 24, 3386-3393. (doi:10.1523/JNEUROS CI.5151-03.2004)
63. Yohro, T. 1977 Structure of the sinus hair follicle in the big-clawed shrew, Sorex unguiculatus. J. Morphol. 153, 333-353. (doi:10.1002/jmor.1051530211)
64. Muchlinski, M. N. 2010 A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals. J. Hum. Evol. 58, 447-473. (doi:10.1016/j.jhevol.2010.01.012)
65. Hyvärinen, H. 1972 On the histology and histochemistry of the snout and vibrissae of the common shrew (Sorex araneus L.). Z. Zellforsch. 124, 445-453. (doi:10.1007/ BF00335250)
66. Goldschmidt-Lange, U. 1975 Über die morphologischen Unterschiede im Aufbau der facialen Vibrissen einiger Säugetierarten. Zool. Anzeiger 5, 417-427.
67. Hyde, J. B. 1957 A comparative study of certain trigeminal components in two soricid shrews, Blarina brevicauda and Sorex cinereus. J. Comp. Neurol. 107, 339-351. (doi:10.1002/cne.901070303)
68. Leitch, D. B., Sarko, D. K. & Catania, K. C. 2008 Cortical organization and sensory pathways in the water shrew. Presentation abstract 78.10/OO15. Washington, DC: Society for Neuroscience.
69. Catania, K. C. & Kaas, J. H. 1997 Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation. J. Comp. Neurol. 387, 215-233. (doi:10.1002/(SICI)1096-9861(19971020)387:2,215::AID-CNE4.3.0.CO;2-3)
70. Stolzenburg, J. U., Reichenbach, A. & Neumann, M. 1989 Size and density of glial and neuronal cells within the cerebral neocortex of various insectivorian species. Glia 2, 78-84. (doi:10.1002/glia.440020203)
71. Naumann, R. K., Anjum, F., Roth-Alpermann, C. & Brecht, M. 2008 Cytoarchitectonic mapping and quantitative anatomy of the Etruscan shrew cortex. Presentation abstract 370.18/LL24. Washington, DC: Society for Neuroscience.
72. Naumann, R. K., Anjum, F., Roth-Alpermann, C. & Brecht, M. Submitted. Cytoarchitecture, areas, and neuron numbers of the Etruscan shrew cortex. J. Comp. Neurol.
73. Wree, A., Lutz, B. & Thole, U. 1992 Volumes of the cytoarchitectonic areas in the rat cerebral cortex. J. Hirnforsch. 33, 545-548.
74. Campi, K. L. & Krubitzer, L. 2010 Comparative studies of diurnal and nocturnal rodents: differences in lifestyle result in alterations in cortical field size and number. J. Comp. Neurol. 518, 4491-4512. (doi:10.1002/cne.22466)
75. Simons, D. J. 1978 Response properties of vibrissa units in rat SI somatosensory neocortex. J. Neurophysiol. 41, 798-820.
76. Catania, K. C. & Remple, M. S. 2002 Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain. Proc. Natl Acad. Sci. USA 99, 5692-5697. (doi:10.1073/pnas.072097999)
77. Hu, J. & Lewin, G. R. 2006 Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J. Physiol. 577, 815-828. (doi:10.1113/jphysiol.2006.117648)
78. Hu, J., Chiang, L. Y., Koch, M. & Lewin, G. R. 2010 Evidence for a protein tether involved in somatic touch. EMBO J. 29, 855-867. (doi:10.1038/emboj.2009.398)
79. Milenkovic, N., Wetzel, C., Moshourab, R. & Lewin, G. R. 2008 Speed and temperature dependences of mechanotransduction in afferent fibers recorded from the mouse saphenous nerve. J. Neurophysiol. 100, 2771-2783. (doi:10.1152/jn.90799.2008)
80. Avery, R. A., Bedford, J. D. & Newcombe, C. P. 1982 The role of thermoregulation in lizard biology: predatory efficiency in a temperate diurnal basker. Behav. Ecol. Sociobiol. 11, 261-267. (doi:10.1007/ BF00299303)
81. Klatzky, R. L. & Lederman, S. J. 2011 Haptic object perception: spatial dimensionality and relation to vision. Phil. Trans. R. Soc. B 366, 3097-3105. (doi:10.1098/ rstb.2011.0153)
82. Catania, K. C. 2011 The sense of touch in the star-nosed mole: from mechanoreceptors to the brain. Phil. Trans. R. Soc. B 366, 3016-3025. (doi:10.1098/rstb.2011.0128)