Abstract
The timing system of weakly electric fishes is vital for many behavioral processes, but the system has been relatively unexplored in Apteronotus albifrons. This paper describes the receptive fields of phase-locked neurons in the midbrain of A. albifrons, in combination with neuroanatomy and electron microscopy (EM) to delineate a phase-locked area in this fish, the magnocellular mesencephalic nucleus (MMN). The MMN was isolated electrophysiologically through the detection of phase-locked field potentials of high amplitude. Single-cell recordings were made with a sharp electrode while a phase-locked modulated stimulus was provided to the fish. Receptive field centers of phase-locked neurons in MMN were consistent with tuberous electroreceptor density maps from previous studies, but no receptive field centers were found in the posterior 50% of the body. Intracellular and extracellular labeling of MMN revealed three cell populations: giant cells with large somata (19–24 µm) and their axonal arborizations which span across the entire extent of MMN, axon terminals from spherical cells of the electrosensory lateral line lobe (ELL), and small cell somata (3–7 µm) along with their projections which extend outside the nucleus. EM revealed multiple gap junction and chemical synapses within MMN. Our results indicate that MMN is a dedicated temporal processing center in A. albifrons.
Similar content being viewed by others
References
Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22(11):4577–4590. https://doi.org/10.1523/JNEUROSCI.22-11-04577.2002
Carr CE, Boudreau RE (1993) An axon with a myelinated initial segment in the bird auditory system. Brain Res 628(1–2):330–334. https://doi.org/10.1016/0006-8993(93)90975-s
Carr CE, Friedman MA (1999) Evolution of time coding systems. Neural Comput 11(1):1–20. https://doi.org/10.1162/089976699300016773
Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211(2):139–153. https://doi.org/10.1002/cne.902110204
Carr CE, Heiligenberg W, Rose GJ (1986a) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6(1):107–119. https://doi.org/10.1523/JNEUROSCI.06-01-00107.1986
Carr CE, Maler L, Taylor B (1986b) A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6(5):1372–1383. https://doi.org/10.1523/JNEUROSCI.06-05-01372.1986
Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature 423(6935):77–81. https://doi.org/10.1038/nature01590
Franchina CR, Hopkins CD (1996) The dorsal filament of the weakly electric Apteronotidae (Gymnotiformes; Teleostei) is specialized for electroreception. Brain Behav Evol 47(4):165–178. https://doi.org/10.1159/000113236
Gerstner W, Kreiter AK, Markram H, Herz AV (1997) Neural codes: firing rates and beyond. Proc Natl Acad Sci USA 94(24):12740–12741. https://doi.org/10.1073/pnas.94.24.12740
Guo YX, Kawasaki M (1997) Representation of accurate temporal information in the electrosensory system of the African electric fish, Gymnarchus niloticus. J Neurosci 17(5):1761–1768. https://doi.org/10.1523/JNEUROSCI.17-05-01761.1997
Kawasaki M (1993) Temporal hyperacuity in the gymnotiform electric fish, Eigenmannia. Ameri Zool 33:86–93
Kawasaki M (2009) Evolution of time-coding systems in weakly electric fishes. Zool Sci 26(9):587–599. https://doi.org/10.2108/zsj.26.587
Kawasaki M, Guo YX (1996) Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus. J Neurosci 16(1):380–391. https://doi.org/10.1523/JNEUROSCI.16-01-00380.1996
Konishi M (1991) Deciphering the Brain’s Codes. Neural Comput 3(1):1–18. https://doi.org/10.1162/neco.1991.3.1.1
Konishi M (2003) Coding of auditory space. Annu Rev Neurosci 26(1):31–55
Lewis JE, Gilmour KM, Moorhead MJ, Perry SF, Markham MR (2014) Action potential energetics at the organismal level reveal a trade-off in efficiency at high firing rates. J Neurosci 34(1):197–201. https://doi.org/10.1523/JNEUROSCI.3180-13.2014
Maler L (2009a) Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 516(5):376–393. https://doi.org/10.1002/cne.22124
Maler L (2009b) Receptive field organization across multiple electrosensory maps. II. Computational analysis of the effects of receptive field size on prey localization. J Comp Neurol 516(5):394–422. https://doi.org/10.1002/cne.22120
Markham MR, Ban Y, McCauley AG, Maltby R (2016) Energetics of sensing and communication in electric fish: a blessing and a curse in the Anthropocene? Integr Comp Biol 56(5):889–900. https://doi.org/10.1093/icb/icw104
Marsálek P, Koch C, Maunsell J (1997) On the relationship between synaptic input and spike output jitter in individual neurons. Proc Natl Acad Sci USA 94(2):735–740. https://doi.org/10.1073/pnas.94.2.735
Martinez D, Metzen MG, Chacron MJ (2016) Electrosensory processing in Apteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species. J Neurophysiol 116(6):2909–2921. https://doi.org/10.1152/jn.00594.2016
Matsushita A, Kawasaki M (2004) Unitary giant synapses embracing a single neuron at the convergent site of time-coding pathways of an electric fish, Gymnarchus niloticus. J Comp Neurol 472(2):140–155. https://doi.org/10.1002/cne.11041
Matsushita A, Pyon G, Kawasaki M (2013) Time disparity sensitive behavior and its neural substrates of a pulse-type gymnotiform electric fish, Brachyhypopomus gauderio. J Comp Physiol A 199(7):583–599. https://doi.org/10.1007/s00359-012-0784-4
Nelson ME, Maciver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202(Pt 10):1195–1203
Réthelyi M, Szabo T (1973) A particular nucleus in the mesencephalon of weakly electric fish, Gymnotus carapo, Gymnotidae. I. Light microscopic structure. Exp Brain Res 17:229–241
Rose GJ, Heiligenberg W (1985) Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity. J Neurosci 5:2269–2280
Somjen G (1972) Sensory coding in the mammalian nervous system. Plenum, New York
Sullivan WE, Konishi M (1984) Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J Neurosci 4(7):1787–1799. https://doi.org/10.1523/JNEUROSCI.04-07-01787.1984
Szabo T (1965) Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae. J Morphol 117(2):229–249. https://doi.org/10.1002/jmor.1051170208
Szabo T (1967) Activity of peripheral and central neurons involved in electroreception. In: Cahn PH (ed) Lateral line detectors. Indiana Univ Press, Bloomington, pp 295–311
Szabo T, Fessard A (1974) Physiology of electroreceptors. In: Fessard A (ed) Handbook of sensory physiology III/3 electroreceptors and other specialized receptors in lower vertebrates. Springer, New York, pp 59–124
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Leonard, J., Matsushita, A. & Kawasaki, M. Morphology and receptive field organization of a temporal processing region in Apteronotus albifrons. J Comp Physiol A 208, 405–420 (2022). https://doi.org/10.1007/s00359-022-01546-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-022-01546-1