Investigation of a Putative Central Sympathetic Pattern Generator in the Frog Spinal Cord
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Abstract
Cardiorespiratory control is essential for survival of all vertebrates, yet our understanding of the neuronal circuits 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. Using 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; (d) persists in a chunk of spinal cord centered around SNIII; and (e) is present in early developmental stages. These data suggest a pair of additional neuronal oscillators in the frog spinal cord located at the level of SNIII. However, removal of the brainstem alters the frequency, increases variability and degrades left-right synchrony of the rhythm, suggesting brainstem connections are important for normal function. We propose that the SNIII rhythm in frog is the output of a central neural oscillator that modulates sympathetic nervous system activity.