Neural control of behavior in knifefish

Many of our investigations relate to the question of how the central nervous system controls behavior. To address this question, we have conducted cell biological, neuroanatomical, neuroendocrinological, and behavioral studies. At the behavioral level, we have focused on a well-defined behavioral pattern exhibited by some weakly electric gymnotiform fish. This behavior, called ‘chirping,’ consists of transient modulations of the otherwise extremely constant electric discharges produced by the fish’s electric organ. We have analyzed the biophysical properties and the functional significance of this behavioral pattern. In the course of our studies, we discovered a novel behavioral response involving the production of chirps; we named this behavior the ‘echo response’.

The brain area that controls chirping is the central posterior/prepacemaker nucleus in the dorsal thalamus. Using a variety of techniques, we have characterized the neuronal organization of this nucleus and its connectivity with other brain regions (see also ‘Research – Neural Connections in the Teleost Nervous System’). Most significantly, we have identified in the central posterior/prepacemaker nucleus several structural correlates of seasonal changes in chirping behavior. The wider implication of these studies are that — contrary to earlier beliefs — the adult brain has an enormous potential to undergo major structural alterations, including growth/retraction of dendrites and even generation of new neurons, to accommodate long-term changes in behavior.

Selected Publications:

Zupanc, G.K.H., Heiligenberg, W.F.: Sexual maturity-dependent changes in neuronal morphology in the prepacemaker nucleus of adult weakly electric knifefish, Eigenmannia. Journal of Neuroscience 9, 3816-3827 (1989), URL: http://www.jneurosci.org/content/9/11/3816

Zupanc, G.K.H.: The synaptic organization of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative ultrastructural study. Journal of Neurocytology 20, 818-833 (1991), doi:10.1007/BF01191733

Zupanc, G.K.H., Zupanc, M.M.: Birth and migration of neurons in the central posterior/prepacemaker nucleus during adulthood in weakly electric knifefish, Eigenmannia sp. Proceedings of the National Academy of Sciences U.S.A. 89, 9539-9543 (1992), URL: http://www.pnas.org/content/89/20/9539

Zupanc, G.K.H., Maler, L.: Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Canadian Journal of Zoology 71, 2301-2310 (1993), doi:10.1139/z93-323

Stroh, T., Zupanc, G.K.H.: Somatostatin in the prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: evidence for a nonsynaptic function. Brain Research 674, 1-14 (1995), doi:10.1016/0006-8993(94)01397-Z

Stroh, T., Zupanc, G.K.H.: The postembryonic development of somatostatin immunoreactivity in the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: a double-labelling study. Developmental Brain Research 93, 76-87 (1996), doi:10.1016/0165-3806(96)00003-X

Zupanc, G.K.H., Horschke, I.: Tectal input to the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: an in vitro tract-tracing study. Brain Research 739, 201-209 (1996), doi:10.1016/S0006-8993(96)00818-9

Zupanc, G.K.H., Horschke, I.: Reciprocal connections between the preglomerular nucleus and the central posterior/prepacemaker nucleus in the diencephalon of weakly electric fish, Apteronotus leptorhynchus. Neuroscience 80, 653‑667 (1997), doi:10.1016/S0306-4522(97)00149-8

Zupanc, G.K.H., Horschke, I.: A distinct population of neurons in the central posterior/prepacemaker nucleus project to the nucleus preopticus periventricularis in the weakly electric gymnotiform fish, Apteronotus leptorhynchus. Brain Research 776, 117-125 (1997), doi:10.1016/S0006-8993(97)01006-8

Zupanc, G.K.H., Maler, L.: Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish. Journal of Comparative Physiology A 180, 99-111 (1997), doi:10.1007/s003590050031

Engler, G., Fogarty, C.M., Banks, J.R., Zupanc, G.K.H.: Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus: a quantitative biophysical and behavioral analysis. Journal of Comparative Physiology A 186, 645-660 (2000), doi:10.1007/s003590000118

Zupanc, G.K.H., Lamprecht, J.: Towards a cellular understanding of motivation: structural reorganization and biochemical switching as key mechanisms ofbehavioral plasticity. Ethology 106, 467-478 (2000), doi:10.1046/j.1439-0310.2000.00546.x

Engler, G., Zupanc, G.K.H.: Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus. Journal of Comparative Physiology A 187, 747-756 (2001), doi:10.1007/s00359-001-0248-8

Zupanc, M.M., Engler, G., Midson, A., Oxberry, H., Hurst, L.A., Symon, M.R., Zupanc, G.K.H.: Light-dark changes in spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus. Animal Behaviour 62, 1119-1128 (2001), doi:10.1006/anbe.2001.1867

Corrêa, S.A.L., Zupanc, G.K.H.: Connections between the central posterior/prepacemaker nucleus and hypothalamic areas in the weakly electric fish Apteronotus leptorhynchus: evidence for an indirect, but not a direct, link. Journal of Comparative Neurology 442, 348-364 (2002), doi:10.1002/cne.10103

Zupanc, G.K.H.: From oscillators to modulators: behavioral and neural control of modulations of the electric organ discharge in the gymnotiform fish, Apteronotus leptorhynchus. Journal of Physiology (Paris) 96, 459-472 (2002), doi:10.1016/S0928-4257(03)00002-0

Zupanc, G.K.H., Corrêa, S.A.L.: Reciprocal neural connections between the central posterior/prepacemaker nucleus and nucleus G in the gymnotiform fish, Apteronotus leptorhynchus. Brain, Behavior and Evolution 65, 14-25 (2005), doi:10.1159/000081107

Zupanc, G.K.H., Sîrbulescu, R.F., Nichols, A., Ilies, I.: Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus. Journal of Comparative Physiology A 192, 159-173 (2006), doi:10.1007/s00359-005-0058-5

Gama Salgado, J.A., Zupanc, G.K.H.: Echo response to chirping in the weakly electric brown ghost knifefish (Apteronotus leptorhynchus): role of frequency and amplitude modulations. Canadian Journal of Zoology 89, 498-508 (2011), doi:10.1139/z11-014

Zupanc, G.K.H., Ilieş, I., Sîrbulescu, R.F., Zupanc, M.M.: Large-scale identification of proteins involved in the development of a sexually dimorphic behavior. Journal of Neurophysiology 111, 1646-1654 (2014), doi:10.1152/jn.00750.2013