Skip to main content
SpringerLink
Log in

A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: anatomical and electrophysiological aspects

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Our long-term goal is to approach the understanding of the anatomical and physiological bases for communication signal diversity in gymnotiform fishes as a model for vertebrate motor pattern generation. Brachyhypopomus gauderio emits, in addition to its electric organ discharge (EOD) at basal rate, a rich repertoire of rate modulations. We examined the structure of the pacemaker nucleus, responsible for the EOD rate, to explore whether its high output signal diversity was correlated to complexity in its neural components or regional organization. We confirm the existence of only two neuron types and show that the previously reported dorsal–caudal segregation of these neurons is accompanied by rostral–caudal regionalization. Pacemaker cells are grouped dorsally in the rostral half of the nucleus, and relay cells are mainly ventral and more abundant in the caudal half. Relay cells are loosely distributed from the center to the periphery of the nucleus in correlation to somata size. Our findings support the hypothesis that regional organization enables a higher diversity of rate modulations, possibly offering distinct target areas to modulatory inputs. Since no anatomical or electrophysiological seasonal or sexual differences were found, we explored these aspects from a functional point of view in a companion article.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

EO:

Electric organ

EOD:

Electric organ discharge

Cd:

Caudal

CV:

Coefficient of variation

Dr:

Dorsal

EBST:

Electromotor bulb spinal tract

PM:

Pacemaker neurons

PN:

Pacemaker nucleus

PPNc:

Diencephalic prepacemaker chirp region

R:

Relay neurons

Rt:

Rostral

sPPN:

Sublemniscal prepacemaker

Vt:

Ventral

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with image. J Biophotonics Int 11:36–42

    Google Scholar 

  • Bass A (1989) Evolution of vertebrate motor systems for acoustic and electric communication: peripheral and central elements. Brain Behav Evol 33:237–247

    Article  CAS  PubMed  Google Scholar 

  • Bennett MVL (1966) Physiology of electrotonic junctions. Ann N Y Acad Sci 137:509–539

    Article  CAS  PubMed  Google Scholar 

  • Bennett MVL (1971) Electroreception. In: Hoar W, Randall D (eds) Fish physiology. Academic Press, New York, pp 493–574

    Google Scholar 

  • Bennett MVL, Pappas GD, Gimenez M, Nakajima Y (1967) Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 30:236–300

    CAS  PubMed  Google Scholar 

  • Bugajska-Schretter A, Grote M, Vangelista L, Valenta R, Sperr WR, Rumpold H, Pastore A, Reichelt R, Valenta R, Spitzauer S (2000) Purification, biochemical, and immunological characterization of a major food allergen: different immunoglobulin E recognition of the apo- and calcium-bound forms of carp parvalbumin. Gut 46:661–669

    Article  CAS  PubMed  Google Scholar 

  • Caceres A, Binder L, Payne MR, Bender P, Rebhun L, Steward O (1984) Differential subcellular localization of tubulin and the microtubule-associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies. J Neurosci 4:394–410

    Google Scholar 

  • Curti S, Falconi A, Morales FR, Borde M (1999) Mauthner cell-initiated electromotor behavior is mediated via NMDA and metabotropic glutamatergic receptors on medullary pacemaker neurons in a Gymnotid fish. J Neurosci 19:9133–9140

    CAS  PubMed  Google Scholar 

  • Curti S, Comas V, Rivero C, Borde M (2006) Analysis of behavior-related excitatory inputs to a central pacemaker nucleus in a weakly electric fish. Neuroscience 140:491–504

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD, Larkins-Ford J (2003) Diversity in the structure of electrocommunication signals within a genus of electric fish, Apteronotus. J Comp Physiol A 189:153–161

    CAS  Google Scholar 

  • Dye J (1991) Ionic and synaptic mechanisms underlying a brainstem oscillator: an in vitro study of the pacemaker nucleus of Apteronotus. J Comp Physiol A 168:521–532

    Article  CAS  PubMed  Google Scholar 

  • Dye J, Meyer J (1986) Central control of the electric organ discharge in weakly electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 71–102

    Google Scholar 

  • Dye J, Heiligenberg W, Keller CH, Kawasaki M (1989) Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Proc Natl Acad Sci USA 86:8993–8997

    Article  CAS  PubMed  Google Scholar 

  • Elekes K, Szabo T (1981) Comparative synaptology of the pacemaker (command) nucleus of the brain of weakly electric fish (Gymnotidae). In: Szabo T, Czéh G (eds) Sensory physiology of aquatic lower vertebrates. Akadémiai Kiadó/Pergamon Press, Budapest/Oxford, pp 107–128

    Google Scholar 

  • Elekes K, Szabo T (1985) Synaptology of the medullary command (pacemaker) nucleus of the weakly electric fish (Apteronotus leptorhynchus) with particular reference to comparative aspects. Exp Brain Res 60:509–520

    Article  CAS  PubMed  Google Scholar 

  • Ellis DB, Szabo T (1980) Identification of different cells types in the command (pacemaker) nucleus of several gymnotiform species by retrograde transport of horseradish peroxidase. Neuroscience 5:1917–1929

    Article  CAS  PubMed  Google Scholar 

  • Engler G, Fogarty C, Banks J, Zupanc GKH (2000) Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apternotus leptorhynchus: a biophysical and behavioral analysis. J Comp Physiol A 186:645–660

    Article  CAS  PubMed  Google Scholar 

  • Giora JL, Malabarba LR (2009) Brachyhypopomus gauderio, new species, a new example of underestimated species diversity of electric fishes in the southern South America (Gymnotiformes: Hypopomidae). Zootaxa 2093:60–68

    Google Scholar 

  • Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263–277

    Article  CAS  PubMed  Google Scholar 

  • Hagedorn M (1988) Ecology and behavior of a pulse type electric fish Hypopomus occidentalis (Gymnotiformes, Hypopomidae) in a fresh-water stream in Panama. Copeia 2:324–335

    Article  Google Scholar 

  • Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gimnotoid fish. Anim Behav 33:254–265

    Article  Google Scholar 

  • Heiligenberg W (1986) Jamming avoidance response: model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–649

    Google Scholar 

  • Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28:560–580

    CAS  PubMed  Google Scholar 

  • Hope BT, Vincent SR (1989) Histochemical characterization of neuronal NADPH-diaphorase. J Histochem Cytochem 37:653–661

    CAS  PubMed  Google Scholar 

  • Hopkins CD (1972) Sex differences in electric signaling in an electric fish. Science 176:1035–1037

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CD (1974a) Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50:270–305

    Article  Google Scholar 

  • Hopkins CD (1974b) Electric communication in the reproductive behavior of Sternopygus macrurus (Gymnotoidei). Z Tierpsychol 35:518–535

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CD (1988) Neuroethology of electric communication. Annu Rev Neurosci 11:497–535

    Article  CAS  PubMed  Google Scholar 

  • Hupé GJ, Lewis JE (2008) Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus. J Exp Biol 211:1657–1667

    Article  PubMed  Google Scholar 

  • Juranek J, Metzner W (1998) Segregation of behavior-specific synaptic inputs to a vertebrate neuronal oscillator. J Neurosci 18:9010–9019

    CAS  PubMed  Google Scholar 

  • Kawasaki M, Heiligenberg W (1989) Distinct mechanisms of modulation in a neuronal oscillator generate different signals in the electric fish Hypopomus. J Comp Physiol A 165:731–741

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki M, Heiligenberg W (1990) Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish. J Neurosci 10:3896–3904

    CAS  PubMed  Google Scholar 

  • Kawasaki M, Maler L, Rose GJ, Heiligenberg W (1988) Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neurol 276:113–131

    Article  CAS  PubMed  Google Scholar 

  • Keller CH, Kawasaki M, Heiligenberg W (1991) The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus. J Comp Physiol A 169:441–450

    Article  CAS  PubMed  Google Scholar 

  • Kennedy G, Heiligenberg W (1994) Ultrastructural evidence of GABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish, Hypopomus. J Comp Physiol A 174:267–280

    Article  CAS  PubMed  Google Scholar 

  • Libouban S, Szabo T, Ellis D (1981) Comparative study of the medullary command (pacemaker) nucleus in species of the four weakly electric fish families. In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates. Akadémiai Kiadó/Pergamon Press, Budapest/Oxford, pp 95–106

    Google Scholar 

  • Lorenzo D, Sierra F, Silva A, Macadar O (1990) Spinal mechanisms of electric organ discharge synchronization in Gymnotus carapo. J Comp Physiol A 167:447–452

    Article  Google Scholar 

  • Lorenzo D, Sierra F, Silva A, Macadar O (1993) Spatial distribution of the medullary command signal within the electric organ of Gymnotus carapo. J Comp Physiol A 173:221–226

    Article  Google Scholar 

  • Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13:1862–1878

    CAS  PubMed  Google Scholar 

  • Perrone R, Macadar O, Silva A (2009) Social electric signals in freely moving dyads of Brachyhypopomus pinnicaudatus. J Comp Physiol A 195:501–514

    Article  Google Scholar 

  • Quintana L, Silva A, Berois N, Macadar O (2004) Temperature induces gonadal maturation and affects electrophysiological sexual maturity indicators in Brachyhypopomus pinnicaudatus from the temperate climate. J Exp Biol 207:1843–1853

    Google Scholar 

  • Quintana L, Sierra F, Silva A, Macadar O (2010) A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: functional aspects revealed by glutamate stimulation. J Comp Physiol A (in revision)

  • Silva A, Quintana L, Galeano M, Errandonea P, Macadar O (1999) Water temperature sensitivity of EOD waveform in Brachyhypopomus pinnicaudatus. J Comp Physiol A 185:187–197

    Article  Google Scholar 

  • Silva A, Quintana L, Galeano M, Errandonea P (2003) Biogeography and breeding in Gymnotiformes from Uruguay. Environm Biol Fish 66:329–338

    Google Scholar 

  • Silva A, Quintana L, Perrone R, Sierra F (2008) Sexual and seasonal plasticity in the emission of social electric signals. Behavioral approach and neural bases. J Physiol Paris 102:272–278

    Google Scholar 

  • Smith GT, Lu Y, Zakon HH (2000) Parvocells: a novel interneuron type in the pacemaker nucleus of a weakly electric fish. J Comp Neurol 423:427–439

    Article  CAS  PubMed  Google Scholar 

  • Solessio E, Vigh J, Cuenca N, Rapp K, Lasater EM (2002) Membrane properties of an unusual intrinsically oscillating, wide-field teleost retinal amacrine cell. J Physiol 544:831–847

    Article  CAS  PubMed  Google Scholar 

  • Spiro JE (1997) Differential activation of glutamate receptor subtypes on a single class of cells enables a neural oscillator to produce distinct behaviors. J Neurophysiol 78:835–847

    CAS  PubMed  Google Scholar 

  • Spiro JE, Brose N, Heinemann SF, Heiligenberg W (1994) Immunolocalization of NMDA receptors in the central nervous system of weakly electric fish: functional implications for the modulation of a neuronal oscillator. J Neurosci 14:6289–6299

    CAS  PubMed  Google Scholar 

  • Stoddard PK (2002) Electric signals: predation, sex, and environmental constraints. Adv Stud Behav 31:201–242

    Article  Google Scholar 

  • Szabo T, Enger P (1964) Pacemaker activity of the medullary nucleus controlling electric organs in high-frequency gymnotid fish. J Comp Physiol A 49:285–300

    Google Scholar 

  • Thomas E, Pearse AG (1961) The fine localization of dehydrogenases in the nervous system. Z Zellforch Microsk Anat Histochem 2:266–282

    Google Scholar 

  • Tomasiewicz HG, Wood JG (1999) Characterization of microtubule-associated proteins in teleosts. Cell Motil Cytoskeleton 44:155–167

    Article  CAS  PubMed  Google Scholar 

  • Turner RW, Moroz LL (1995) Localization of nicotinamide adenine dinucleotide phosphate-diaphorase activity in electrosensory and electromotor systems of a gymnotiform teleost, Apteronotus leptorhynchus. J Comp Neurol 356:261–274

    Article  CAS  PubMed  Google Scholar 

  • Xiao T, Roeser T, Staub W, Baier H (2005) A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132:2955–2967

    Article  CAS  PubMed  Google Scholar 

  • Zupanc MM, Engler G, Midson A, Oxberry H, Hurst LA, Symon MR, Zupanc GK (2001) Light–dark controlled changes in modulations of the electric organ discharge in teleost Apteronotus leptorhynchus. Anim Behav 62:1119–1128

    Article  Google Scholar 

  • Zupanc GK, Sîrbulescu RF, Nichols A, Ilies I (2006) Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 192:159–173

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Omar Trujillo, Kent Dunlap and Phil Stoddard for their generous revision and suggestions to our manuscript. We thank Catherine Carr for her valuable comments and Amalia Dutra, Hugo Peluffo and Angel Caputi who very kindly donated antibodies used in this study. We are grateful to Rossana Perrone and Ana Silva who performed the behavioral experiments and participated in all field trips. All procedures with animals were performed in accordance with the guidelines of the local ethical committee (Comisión Honoraria de Experimentación Animal, CHEA, Universidad de la República, Uruguay). This research was financed by PDT 043 and PEDECIBA.

Author information

Author notes

  1. Gabriela Fabbiani

    Present address: Dpto de Neurofisiología Celular y Molecular, Instituto de Investigaciones Biológicas Clemente Estable, Avda Italia 3318, 11600, Montevideo, Uruguay

Authors and Affiliations

  1. Dpto de Neurofisiología, Instituto de Investigaciones Biológicas Clemente Estable, Avda Italia 3318, 11600, Montevideo, Uruguay

    Laura Quintana, Paula Pouso, Gabriela Fabbiani & Omar Macadar

  2. Dpto de Histología y Embriología, Facultad de Medicina, Universidad de la República, Gral Flores 2125, 11800, Montevideo, Uruguay

    Paula Pouso

Authors
  1. Laura Quintana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Pouso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela Fabbiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Omar Macadar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Quintana.

Electronic supplementary material

Below is the link to the electronic supplementary material.

3D representation of the PN of Brachyhypopomus gauderio. In a frontal view the PN is tilted slightly counter clockwise. Rostral: indicated with a star. Red pacemaker cells, cyan relay cells.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quintana, L., Pouso, P., Fabbiani, G. et al. A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: anatomical and electrophysiological aspects. J Comp Physiol A 197, 75–88 (2011). https://doi.org/10.1007/s00359-010-0588-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-010-0588-3

Keywords

Search

Navigation