Segregation of Behavior-Specific Synaptic Inputs to a Vertebrate Neuronal Oscillator

Abstract

Although essential for understanding the mechanisms underlying sensorimotor integration and motor control of behaviors, very little is known about the degree to which different behaviors share neural elements of the sensorimotor command chain by which they are controlled. Here, we provide, to our knowledge, the first direct physiological evidence that various modulatory premotor inputs to a vertebrate central pattern generator, the pacemaker nucleus in gymnotiform electric fish, carrying distinctly different behavioral information, can remain segregated from their various sites of origin in the diencephalon to the synaptic termination sites on different target neurons in the medullary pacemaker nucleus. During pharmacological activation of each of the premotor inputs originating from the three prepacemaker nuclei so far identified, we determined in vivo the changes in input resistance in the neuronal elements of the pacemaker nucleus, i.e., relay cells and pacemaker cells. We found that each input yields significantly different effects on these cells; the inputs from the two diencephalic prepacemaker nuclei, PPnC and PPnG, which resulted in increased oscillator activity, caused significantly lower input resistances in relay and pacemaker cells, respectively, exhibiting drastically different time courses. The input from the sublemniscal prepacemaker nucleus, which resulted in reduced oscillator activity, however, caused a significant increase in input resistance only in relay cells. Considering that the sensory pathways processing stimuli yielding these behaviors are separated as well, this study indicates that sensorimotor control of different behaviors can occur in strictly segregated channels from the sensory input of the brain all through to the synaptic input level of the final premotor command nucleus.