NMDAR-dependent control of call duration in Xenopus laevis

J Neurophysiol. 2010 Jun;103(6):3501-15. doi: 10.1152/jn.00155.2010. Epub 2010 Apr 14.

Abstract

Many rhythmic behaviors, such as locomotion and vocalization, involve temporally dynamic patterns. How does the brain generate temporal complexity? Here, we use the vocal central pattern generator (CPG) of Xenopus laevis to address this question. Isolated brains can elicit fictive vocalizations, allowing us to study the CPG in vitro. The X. laevis advertisement call is temporally modulated; calls consist of rhythmic click trills that alternate between fast (approximately 60 Hz) and slow (approximately 30 Hz) rates. We investigated the role of two CPG nuclei--the laryngeal motor nucleus (n.IX-X) and the dorsal tegmental area of the medulla (DTAM)--in setting rhythm frequency and call durations. We discovered a local field potential wave in DTAM that coincides with fictive fast trills and phasic activity that coincides with fictive clicks. After disrupting n.IX-X connections, the wave persists, whereas phasic activity disappears. Wave duration was temperature dependent and correlated with fictive fast trills. This correlation persisted when wave duration was modified by temperature manipulations. Selectively cooling DTAM, but not n.IX-X, lengthened fictive call and fast trill durations, whereas cooling either nucleus decelerated the fictive click rate. The N-methyl-d-aspartate receptor (NMDAR) antagonist dAPV blocked waves and fictive fast trills, suggesting that the wave controls fast trill activation and, consequently, call duration. We conclude that two functionally distinct CPG circuits exist: 1) a pattern generator in DTAM that determines call duration and 2) a rhythm generator (spanning DTAM and n.IX-X) that determines click rates. The newly identified DTAM pattern generator provides an excellent model for understanding NDMAR-dependent rhythmic circuits.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways
  • Animals
  • Evoked Potentials / drug effects
  • Evoked Potentials / physiology
  • Excitatory Amino Acid Antagonists / pharmacology
  • In Vitro Techniques
  • Laryngeal Nerves / physiology*
  • Medulla Oblongata / cytology*
  • Medulla Oblongata / drug effects
  • Neurons / drug effects
  • Neurons / physiology
  • Periodicity
  • Receptors, N-Methyl-D-Aspartate / physiology*
  • Serotonin / pharmacology
  • Temperature
  • Time Factors
  • Valine / analogs & derivatives
  • Valine / pharmacology
  • Vocalization, Animal / drug effects
  • Vocalization, Animal / physiology*
  • Xenopus laevis / physiology*

Substances

  • Excitatory Amino Acid Antagonists
  • Receptors, N-Methyl-D-Aspartate
  • Serotonin
  • 2-amino-5-phosphopentanoic acid
  • Valine