Sensory activation and role of inhibitory reticulospinal neurons that stop swimming in hatchling frog tadpoles.
Activity in neuronal networks underlying locomotion and other rhythmic actions can start and stop in response to specific sensory stimuli. In vertebrate locomotion, some reticulospinal neurons such as Mauthner neurons can initiate activity, but the neurons controlling stopping are not defined. We have studied swimming in tadpoles of the frog, Xenopus, which is started by touching the skin and stops when the head contacts a solid surface. Using an immobilized tadpole preparation, the same stimuli control fictive swimming. When head contact is imitated by pressure to the head skin sensory neurons in the trigeminal ganglion are active, spinal neurons receive GABAergic inhibition, and swimming stops. Here we record intracellularly from neurons in the hindbrain that are excited by pressure or electrical stimulation to the head skin. By intracellular filling with neurobiotin, we identify these anatomically as mid-hindbrain reticulospinal neurons (MHRs). These have contralateral descending projections to the spinal cord and GABA-like immunoreactivity. They are rhythmically inhibited during fictive swimming. Individual MHRs reliably stopped ongoing swimming when brief firing was induced by intracellular current injection. The ability of individual MHRs to stop swimming was blocked by the GABA(A) antagonist bicuculline. Our evidence indicates that MHRs receive direct excitation from trigeminal sensory neurons and in turn release GABA to directly inhibit spinal neurons and turn off the swimming central pattern generator.
Perrins
Ray
R
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom.
Walford
Alison
A
Roberts
Alan
A
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001710:Biotin / Q000031:analogs & derivatives*; D004558:Electric Stimulation; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D018682:GABA Agents / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D058787:GABA-A Receptor Antagonists; D007814:Larva / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D008839:Microelectrodes; D009433:Neural Inhibition / Q000187:drug effects / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology; D009474:Neurons / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D010507:Periodicity; D010812:Physical Stimulation / Q000379:methods; D011312:Pressure; D011930:Reaction Time / Q000502:physiology; D012249:Rhombencephalon / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D013116:Spinal Cord / Q000502:physiology; D013331:Strychnine / Q000494:pharmacology; D013550:Swimming / Q000502:physiology*; D014982:Xenopus laevis
D018691:Excitatory Amino Acid Antagonists; D018682:GABA Agents; D018756:GABA Antagonists; D058787:GABA-A Receptor Antagonists; C070614:neurobiotin; D001710:Biotin; D013331:Strychnine