More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii

Amey-Özel M, von der Emde G, Engelmann J, Grant K (2015)
The Journal of comparative neurology 523(5): 769-789.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Amey-Özel, Monique; von der Emde, Gerhard; Engelmann, JacobUniBi ; Grant, Kirsty
Abstract / Bemerkung
The weakly electric fish Gnathonemus petersii uses its electric sense to actively probe the environment. Its highly mobile chin appendage, the Schnauzenorgan, is rich in electroreceptors. Physical measurements have demonstrated the importance of the position of the Schnauzenorgan in funneling the fish's self-generated electric field. The present study focuses on the trigeminal motor pathway that controls Schnauzenorgan movement and on its trigeminal sensory innervation and central representation. The nerves entering the Schnauzenorgan are very large and contain both motor and sensory trigeminal components as well as an electrosensory pathway. With the use of neurotracer techniques, labeled Schnauzenorgan motoneurons were found throughout the ventral main body of the trigeminal motor nucleus but not among the population of larger motoneurons in its rostrodorsal region. The Schnauzenorgan receives no motor or sensory innervation from the facial nerve. There are many anastomoses between the peripheral electrosensory and trigeminal nerves, but these senses remain separate in the sensory ganglia and in their first central relays. Schnauzenorgan trigeminal primary afferent projections extend throughout the descending trigeminal sensory nuclei, and a few fibers enter the facial lobe. Although no labeled neurons could be identified in the brain as the trigeminal mesencephalic root, some Schnauzenorgan trigeminal afferents terminated in the trigeminal motor nucleus, suggesting a monosynaptic, possibly proprioceptive, pathway. In this first step toward understanding multimodal central representation of the Schnauzenorgan, no direct interconnections were found between the trigeminal sensory and electromotor command system, or the electrosensory and trigeminal motor command. The pathways linking perception to action remain to be studied. J. Comp. Neurol. 523:769-789, 2015. © 2014 Wiley Periodicals, Inc.
Erscheinungsjahr
2015
Zeitschriftentitel
The Journal of comparative neurology
Band
523
Ausgabe
5
Seite(n)
769-789
ISSN
1096-9861
Page URI
https://pub.uni-bielefeld.de/record/2718911

Zitieren

Amey-Özel M, von der Emde G, Engelmann J, Grant K. More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii. The Journal of comparative neurology. 2015;523(5):769-789.
Amey-Özel, M., von der Emde, G., Engelmann, J., & Grant, K. (2015). More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii. The Journal of comparative neurology, 523(5), 769-789. doi:10.1002/cne.23710
Amey-Özel, Monique, von der Emde, Gerhard, Engelmann, Jacob, and Grant, Kirsty. 2015. “More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii”. The Journal of comparative neurology 523 (5): 769-789.
Amey-Özel, M., von der Emde, G., Engelmann, J., and Grant, K. (2015). More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii. The Journal of comparative neurology 523, 769-789.
Amey-Özel, M., et al., 2015. More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii. The Journal of comparative neurology, 523(5), p 769-789.
M. Amey-Özel, et al., “More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii”, The Journal of comparative neurology, vol. 523, 2015, pp. 769-789.
Amey-Özel, M., von der Emde, G., Engelmann, J., Grant, K.: More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii. The Journal of comparative neurology. 523, 769-789 (2015).
Amey-Özel, Monique, von der Emde, Gerhard, Engelmann, Jacob, and Grant, Kirsty. “More a finger than a nose: The trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose Fish Gnathonemus petersii”. The Journal of comparative neurology 523.5 (2015): 769-789.

82 References

Daten bereitgestellt von Europe PubMed Central.


AUTHOR UNKNOWN, 0

Ariéns-Kappers, 1967
Functional foveae in an electrosensory system.
Bacelo J, Engelmann J, Hollmann M, von der Emde G, Grant K., J. Comp. Neurol. 511(3), 2008
PMID: 18803238
Respiratory neurons in rainbow trout (Salmo gairdneri)
Bamford, Comp Biochem Physiol 48A(), 1974

Bell, 1986
Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: II
Bell, Intra-axonal recordings show initial stages of central processing. J Neurophysiol 63(), 1990

Bell, 1986
Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish.
Bell CC, Libouban S, Szabo T., J. Comp. Neurol. 216(3), 1983
PMID: 6306068
Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology.
Bell CC, Zakon H, Finger TE., J. Comp. Neurol. 286(3), 1989
PMID: 2768566
Sensory processing and corollary discharge effects in the mormyromast regions of the mormyrid electrosensory lobe
Bell, I. Field potentials, cellular activity in associated structures. J Neurophysiol 68(), 1992
Electroreceptors in mormyrids.
Bennett MV., Cold Spring Harb. Symp. Quant. Biol. 30(), 1965
PMID: 5219479
The central relations of the cranial nerves in Silurus glanis and Mormyrus caschive
Berkelbach, J Comp Neurol 25(), 1915
Sensory and autonomic innervation of non-hairy and hairy human skin. An immunohistochemical study.
Bjorklund H, Dalsgaard CJ, Jonsson CE, Hermansson A., Cell Tissue Res. 243(1), 1986
PMID: 2417723
Schreiner organs: a new craniate chemosensory modality in hagfishes.
Braun CB., J. Comp. Neurol. 392(2), 1998
PMID: 9512266

Butler, 2005
Trigeminal projections to the dorsal thalamus in a lacertid lizard, Podarcis hispanica.
Desfilis E, Font E, Garcia-Verdugo JM., Brain Behav. Evol. 52(2), 1998
PMID: 9681163
The Schnauzenorgan-response of Gnathonemus petersii.
Engelmann J, Nobel S, Rover T, Emde GV., Front. Zool. 6(), 2009
PMID: 19772622

Faverger, 1981
The regulation of motile activity in fish chromatophores.
Fujii R., Pigment Cell Res. 13(5), 2000
PMID: 11041206
Control of the melanophores of the minnow (Phoxinus phoxinus (L.))
Gray, J Exp Biol 33(), 1956
Die Beziehungen zwischen Elektrorezeptoren, elektrischem Organ, Seitenlinienorganen und Nervensystem bei den Mormyridae (Teleostei, Pisces)
Harder, Z vergl Phys 59(), 1968
Topological analysis of the brainstem of the bowfin, Amia calva.
Heijdra YF, Nieuwenhuys R., J. Comp. Neurol. 339(1), 1994
PMID: 8106657
The cranial nerves and cutaneous sense organs of the North American Siluroid fishes
Herrick, J Comp Neurol 11(), 1901
The central gustatory paths in the brains of bony fishes
Herrick, J Comp Neurol 15(), 1905
On the centers for taste and touch in the medulla oblongata of fishes
Herrick, J Comp Neurol 16(), 1906
Distribution, density and morphology of electroreceptor organs in mormyrid weakly electric fish: anatomical investigations of a receptor mosaic
Hollmann, J Zool 276(), 2008

Iwata, 1973
Central distribution of trigeminal primary afferent fibers in anuran amphibians.
Joseph BS, King RB, Whitlock DG., Anat. Rec. 160(4), 1968
PMID: 5666661
Somatotopic organization of the trigeminal ganglion cells in a cichlid fish, Oreochromis (Tilapia) niloticus.
Kerem G, Yoshimoto M, Yamamoto N, Yang CY, Xue HG, Ito H., Brain Behav. Evol. 65(2), 2004
PMID: 15627723
Distribution of trigeminal fibers in the primary facial gustatory center of channel catfish, Ictalurus punctatus.
Kiyohara S, Yamashita S, Lamb CF, Finger TE., Brain Res. 841(1-2), 1999
PMID: 10546992

Kleiser, 1993
A method for the combined staining of cells and fibers in the nervous system.
KLUVER H, BARRERA E., J. Neuropathol. Exp. Neurol. 12(4), 1953
PMID: 13097193
The origin of the cranial ganglia in Amiurus
Landacre, J Comp Neurol 20(), 1910
On the occurrence of Merkel cells in the epidermis of teleost fishes.
Lane EB, Whitear M., Cell Tissue Res. 182(2), 1977
PMID: 198137
Neurobiology of orofacial proprioception.
Lazarov NE., Brain Res Rev 56(2), 2007
PMID: 17915334

AUTHOR UNKNOWN, 0

Lorenzini, 1678
The central connections of the posterior lateral line nerve of Gnathonemus petersii.
Maler L, Karten HJ, Bennett MV., J. Comp. Neurol. 151(1), 1973
PMID: 4731302
The central connections of the anterior lateral line nerve of Gnathonemus petersii.
Maler L, Karten HJ, Bennett MV., J. Comp. Neurol. 151(1), 1973
PMID: 4731303

Meek, 1998
Structural organization of the mormyrid electrosensory lateral line lobe
Meek J, Grant K, Bell C., J. Exp. Biol. 202(# (Pt 10)), 1999
PMID: 10210669

Merkel, 1880
Behavioral measurements of sensory gating by a corollary discharge
Meyer, J Comp Physiol 151(), 1983
The double innervation of fish melanophores
Mills, J Exp Zool 64(), 1932
The response of the Ampullae of Lorenzini of elasmobranchs to mechanical stimulation
Murray, J Exp Biol 37(), 1960
Somatotopic organization of the primary sensory trigeminal neurons in the hagfish, Eptatretus burgeri.
Nishizawa H, Kishida R, Kadota T, Goris RC., J. Comp. Neurol. 267(2), 1988
PMID: 3343402
Action of melanin-concentrating hormone (MCH) on teleost chromatophores.
Oshima N, Kasukawa H, Fujii R, Wilkes BC, Hruby VJ, Hadley ME., Gen. Comp. Endocrinol. 64(3), 1986
PMID: 3026881
Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation.
Pusch R, von der Emde G, Hollmann M, Bacelo J, Nobel S, Grant K, Engelmann J., J. Exp. Biol. 211(Pt 6), 2008
PMID: 18310118
Occurrence of sensory nerve endings (stretch receptors) in muscles of a teleost, Gnathonemus petersii
Srivastava, Natl Acad Sci Lett 2(), 1979
Morphologische Studien an Mormyriden
Stendell, Verh Dtsch Zool Ges 24(), 1914
Die Schnauzenorgane der Mormyriden
Stendell, Zeit Wiss Zool 115(), 1916
Über eine bisher unbekannte Funktion der sogenannten ampullären Organe bei Gnathonemus petersii
Szabo, J Comp Physiol 66(), 1970
Le fonctionnement des électrorécepteurs étudié chez les Mormyres
Szabo, J Physiol Paris 57(), 1965
Cerebellar afferents in weakly electric mormyrid fish
Szabo, Neurosci Lett S3(), 1979
Imaging of objects through active electrolocation in Gnathonemus petersii.
von der Emde G, Schwarz S., J. Physiol. Paris 96(5-6), 2002
PMID: 14692491
Active electrolocation in Gnathonemus petersii: behaviour, sensory performance, and receptor systems.
von der Emde G, Amey M, Engelmann J, Fetz S, Folde C, Hollmann M, Metzen M, Pusch R., J. Physiol. Paris 102(4-6), 2008
PMID: 18992334
Beiträge zur Physiologie der Pigmentzellen in der Fischhaut
Frisch, Pflügers Arch Eur J Physiol Bd 138(), 1911

Waite, 2004
The mesencephalic root of the fifth nerve. A comparative anatomical study
Weinberg, J Comp Neurol 46(), 1928
Physiological salines for freshwater teleosts
Wolf, Progr Fish Cult 25(), 1963
A phylogenetic consideration of the primary and secondary centers and connections of the trigeminal complex in a series of vertebrates
Woodburne, J Comp Neurol 65(), 1936
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 25388854
PubMed | Europe PMC

Suchen in

Google Scholar