Putative Sympathetic Oscillator in the Thoracic Spinal Cord of the Bullfrog

Abstract

BACKGROUNDCardiorespiratory control is essential for survival of all vertebrates, yet our understanding of the neuronal circuitry involved is rudimentary ‐‐ in part because there is little data beyond mammals to guide us. Neuronal oscillators are discrete neural circuits located within the central nervous system that are capable of generating rhythmic outputs without phasic input. These circuits are found throughout the animal kingdom and are often critical for regulating overt rhythmic behaviours such breathing. Previously, we found three oscillators in the frog brainstem that control ventilation: one for buccal ventilation, two for lung. Three respiratory oscillators have subsequently been found in mammals. Central neuronal oscillators within the sympathetic nervous system of frogs and mammals have also been suspected, but these oscillators have yet to be precisely located.FINDINGSUsing extracellular recording and transection techniques in the frog superfused, isolated brainstem and spinal cord preparation, we discovered a robust, yet previously unreported buccal‐like rhythm in the third spinal nerve (SNIII). Unlike the ventilatory rhythms we normally study, the SNIII rhythm demonstrates poor bilateral synchrony. Our data also suggest that this rhythm is: (a) not coupled to ventilatory rhythms recorded in cranial nerves; (b) has distinct responses to pharmacological stimulation compared to ventilatory rhythms; (c) does not require the brainstem; and (d) persists in a chunk of spinal cord centered around SNIII. These data suggest an additional neuronal oscillator in the frog spinal cord located at the level of SNIII. However, removing the brainstem alters the frequency, increases variability and degrades left‐right synchrony of the rhythm, suggesting brainstem connections are important for normal function.SIGNIFICANCEThe literature has long debated the existence of central neuronal oscillators that modulate sympathetic nervous system activity in vertebrates. We propose that the bursting activity recorded from the SNIII in frog is the output of such an oscillator, discovery of which could prove critical in shaping our current understanding of the function and evolution of the sympathetic nervous system.Support or Funding InformationNSERC and HBI.