Abstract
Xenopus laevis employs mechano-sensory lateral lines to, for instance, capture arthropods on the surface of turbid waters with poor visibility based on incoming wave signals. To characterise central representations of surface waves emitted from different locations, responses to several wave parameters were extracellularly recorded across brainstem, midbrain and thalamic areas. Overall, 339 of 411 statistically analysed responses showed significantly altered spike rates during the presentation of surface waves. Of these units, 45.1 % were obtained in the torus semicircularis including its laminar subnucleus (23.3 %) that is known to process auditory cues. Wave parameters contributing to central object representations were indicated by response rates that systematically varied with amplitude (76.3 % of 160 tested units), frequency (74.4 % of 270 tested units), source angle (93.7 % of 79 tested units), or source distance (63.8 % of 218 tested units). Map-like parameter representations were rather diffuse, yet an increased fraction of units tuned to frontal source angles was observed at deeper tissue layers (>180 μm), and an increased fraction of best neuronal responses to low wave frequencies (≤25 Hz) at rostral midbrain sections. Responses to wave frequencies remained largely robust across tested unit samples independent of source angles, and distances (N = 62). In comparison, spatial response characteristics seemed fragile across different wave frequencies in 68.3 % of 41 recordings.
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Abbreviations
- d:
-
Dorsal
- DTEG:
-
Dorsal tegmentum
- F const :
-
Constant-frequency wave
- F mod :
-
Frequency-modulated wave
- l:
-
Lateral
- LL:
-
Lateral line
- m:
-
Medial
- MED:
-
Medulla
- MES:
-
Mesencephalon
- OT:
-
Optic tectum
- SEM:
-
Standard error of the mean
- TL:
-
Torus semicircularis laminaris
- TM:
-
Torus semicircularis magnocellularis
- TP:
-
Torus semicircularis principalis
- TS:
-
Torus semicircularis
- v:
-
Ventral
- VS:
-
Vector strength
- VTEG:
-
Ventral tegmentum
References
Altman JS, Dawes EA (1983) A cobalt study of medullary sensory projections from lateral line nerves, associated cutaneous nerves, and the VIIIth nerve in adult Xenopus. J Comp Neurol 213:310–326
Argac D, Makambi KH, Hartung J (2001) A note on testing the nullity of the between group variance in the one-way random effects model under variance heterogeneity. J Appl Stat 28:215–222
Ariens-Kappers CU, Huber C, Croshy EC (1960) The comparative anatomy of the nervous system of vertebrates, including man, vol 1. Hafner Publishing Company, New York
Bartels M, Münz H, Claas B (1990) Representation of lateral line and electrosensory systems in the midbrain of the axolotl, Ambystoma mexicanum. J Comp Physiol A 167:347–356
Batschelet E (1991) Circular statistics in biology. Academic Press, London
Behrend O, Branoner F, Zhivkov Z, Ziehm U (2006) Neural responses to water surface waves in the midbrain of the aquatic predator Xenopus laevis laevis. Eur J Nsci 23:729–744
Behrend O, Branoner F, Ziehm U, Zhivkov Z (2008) Lateral line units in the amphibian brain could integrate wave curvatures. J Comp Physiol A 194:777–783
Bleckmann H (2004) 3D-orientation with the octavolateralis system. J Physiol Paris 98:53–65
Bleckmann H (2008) Peripheral and central processing of lateral line information. J Comp Physiol A 194:145–158
Bleckmann H, Schwartz E (1982) The functional significance of frequency modulation within a wave train for prey localization in the surface feeding fish Aplocheilus lineatus (Cyprinodontidae). J Comp Physiol A 145:331–339
Bleckmann H, Tittel G, Blübaum-Gronau E (1989a) The lateral line system of surface-feeding fish: anatomy, physiology, and behaviour. In: Coombs S, Görner P, Münz H (eds) The mechano-sensory lateral line: neurobiology and evolution. Springer, New York, pp 501–526
Bleckmann H, Weiss O, Bullock TH (1989b) Physiology of lateral line mechanoreceptive regions in the elasmobranch brain. J Comp Physiol A 164:459–474
Bleckmann H, Breithaupt T, Blickhan R, Tautz J (1991) The time course and frequency content of hydrodynamic events caused by moving fish, frogs, and crustaceans. J Comp Physiol A 168:749–757
Brudermanns B, Elepfandt A (2004) Excellent discrimination of the distance of two simultaneous water wave sources by the clawed frog Xenopus laevis laevis. In: Proceedings of the 97th Congress German Zoological Society, p 100
Buschmann P, Görner P (1990) Distance localization of the center of a surface wave in the clawed toad Xenopus laevis Daudin. Proceedings of the 18th Göttingen Neurobiology Conference, Stuttgart, p 165
Claas B (1993) Wie analysiert das Seitenliniensystem die Laufrichtung von Oberflächenwellen? Habillitation thesis, Universität Bielefeld (in German)
Claas B, Dean J (2006) Prey capture in the African clawed toad (Xenopus laevis): comparison of tuning to visual and lateral line stimuli. J Comp Physiol A 192:1021–1036
Claas B, Münz H (1996) Analysis of surface wave direction by the lateral line system of Xenopus: source localization before and after inactivation of different parts of the lateral line. J Comp Physiol A 178:253–268
Claas B, Münz H, Görner P (1993) Reaction to surface-waves by Xenopus laevis Daudin—are sensory systems other than the lateral-line involved? J Comp Physiol A 172:759–765
Dudkin E, Gruberg E (2003) Nucleus isthmi enhances calcium influx into optic nerve fibre terminals in Rana pipiens. Brain Res 969(1–2):44–52
Edwards CJ, Kelley DB (2001) Auditory and lateral line inputs to the midbrain of an aquatic anuran: neuroanatomic studies Xenopus laevis. J Comp Neurol 438:148–162
Elepfandt A (1982) Accuracy of taxis response to water-waves in the clawed toad (Xenopus-Laevis Daudin) with intact or with lesioned lateral line system. J Comp Physiol 148:535–545
Elepfandt A (1988) Central organization of wave localization in the clawed frog, Xenopus-Laevis. 2. Midbrain topology for wave directions. Brain Behav Evol 31:358–368
Elepfandt A, Seiler B, Aicher B (1985) Water-wave frequency discrimination in the clawed frog, Xenopus-Laevis. J Comp Physiol A 157:255–261
Franosch JM, Sobotka MC, Elepfandt A, van Hemmen JL (2003) Minimal model of prey localization through the lateral-line system. Phys Rev Lett 91(158101):1–4
Franosch JM, Lingenheil M, van Hemmen JL (2005) How a frog can learn what is where in the dark. Phys Rev Lett 95(078106):1–4
Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613–636
Görner P, Mohr C (1989) Stimulus localization in Xenopus: Role of directional sensitivity of lateral line stitches. In: Coombs S, Görner P (eds) The mechano-sensory lateral line: neurobiology and evolution. Springer, New York, pp 543–560
Gruberg E, Dudkin E, Wang Y, Marin G, Salas C, Sentis E, Letelier J, Mpodozis J, Malpeli J, Cui H, Ma R, Northmore D, Udin S (2006) Influencing and interpreting visual input: the role of a visual feedback system. J Neurosci 26(41):10368–10371
Gutsche A, Elepfandt A (2006) Xenopus laevis (African clawed frog) surface prey capture. Herpetol Rev 37:452
Hoin-Radovsky I, Bleckmann H, Schwartz E (1984) Determination of source distance in the surface-feeding fish Pantodon bucholzi (Pantodontidae). Anim Behav 32:840–851
Kita H, Armstrong W (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. J Neurosci Meth 37:141–150
Knudsen EI (2002) Instructed learning in the auditory localization pathway of the barn owl. Nature 417:322–328
Kroese AB, van der Zalm JM, Vandenbercken BJ (1978) Frequency response of the lateral-line organ of Xenopus laevis. Pflügers Arch 375:167–175
Lang H (1980) Surface wave discrimination between prey and nonprey by the back swimmer Notonecta glauca L. (Hemiptera, Heteroptera). Behav Ecol Sociobiol 6:233–246
Lowe DA (1986) Organisation of lateral line and auditory areas in the midbrain of Xenopus laevis. J Comp Neurol 245:498–513
Müller HM (1996) Indications for feature detection with the lateral line organ in fish. Comp Biochem Physiol 114A:257–263
Müller U, Schwartz E (1982) Influence of single neuromasts on prey localizing behavior of surface-feeding fish, Aplocheilus lineatus. J Comp Physiol A 149:399–408
Nikundiwe AM, Nieuwenhuys R (1983) The cell masses in the brainstem of the South African clawed frog Xenopus laevis: a topographical and topological analysis. J Comp Neurol 213:199–219
Reisbeck T (1994) Investigation of processing of wave stimuli in the midbrain of the clawed frog, Xenopus laevis. PhD thesis, University of Konstanz (in German)
Van der Want JJL, Klooster J, Nunes–Cardozo B, de Weerd H, Liem RSB (1997) Tract-tracing in the nervous system of vertebrates using horseradish peroxidase and its conjugates: tracers, chromogens, and stabilization for light and electron microscopy. Brain Res Protoc 1:267–279
Voges K, Bleckmann H (2011) Two-dimensional receptive fields of midbrain lateral line units in the goldfish, Carassius auratus. J Comp Physiol A 197:827–837
Ziehm U (2006) Lateral line mediated object localization by somatotopic mapping of the azimuth in Xenopus laevis—a modelling approach. Diploma thesis, Humboldt Universität zu Berlin
Zittlau KE, Claas B, Münz H (1986) Directional sensitivity of lateral line units in the clawed toad Xenopus laevis Daudin. J Comp Physiol A 158:469–477
Zöfel P (1988) Statistik in der Praxis (in German). Fischer, Stuttgart, pp 103–105
Acknowledgments
Supported by the Deutsche Forschungsgemeinschaft (DFG; BE 3755/1-1; O. Behrend; F. Branoner), the Bundesministerium für Bildung und Forschung (BMBF; O. Behrend), the Bernstein Center for Computational Neurosciences Berlin (BCCN; U. Ziehm), and the Nachwuchsförderungsgesetz Berlin (NaFöG; Z. Zhivkov). We are indebted to U. Schneeweiss and A. Elepfandt for technical and instrumental support. Experiments were approved by the Landesamt für Gesundheit und Soziales Berlin, and comply with the principles of animal care (publication no. 86–23, revised 1985, of the National Institute of Health).
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Branoner, F., Zhivkov, Z., Ziehm, U. et al. Central representation of spatial and temporal surface wave parameters in the African clawed frog. J Comp Physiol A 198, 797–815 (2012). https://doi.org/10.1007/s00359-012-0749-7
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DOI: https://doi.org/10.1007/s00359-012-0749-7