Descending Control of Turning Locomotor Activity in Larval Lamprey: Neurophysiology and Computer Modeling

Abstract

McClellan, Andrew D. and André Hagevik. Descending control of turning locomotor activity in larval lamprey: neurophysiology and computer modeling. J. Neurophysiol. 78: 214–228, 1997. The purpose of the present study was to examine the mechanisms that produce natural spontaneous turning maneuvers in larval lamprey. During swimming, spontaneous turning movements began with a larger-than-normal bending of the head to one side. Subsequently, undulations propagated down the body with greater amplitude on the side ipsilateral to the turn. During turning to one side, which usually occurred within one cycle, the amplitude and duration of ipsilateral muscle burst activity as well as overall cycle time increased significantly with increasing turn angle. In in vitro brain/spinal cord preparations, brief electrical stimulation applied to the left side of the oral hood at the onset of locomotor burst activity on the right side of the spinal cord produced turninglike motor activity. During the perturbed cycle, the duration and amplitude of the burst on the right as well as cycle time were significantly larger than during preceding control cycles. In several lower vertebrates, unilateral stimulation in brain stem locomotor regions elicits asymmetric, turninglike locomotor activity. In the lamprey, unilateral chemical microstimulation in brain stem locomotor regions elicited continuous asymmetric locomotor activity, but there was little change in cycle time, as occurs during the single turning cycles in whole animals. The descending mechanisms responsible for producing turning locomotor activity were examined with the use of a computer model consisting of left and right phase oscillators in the spinal cord that were coupled by net reciprocal inhibition. With relatively weak reciprocal coupling, a brief unilateral descending excitatory input to one oscillator produced effects ipsilaterally, but there was little effect on the contralateral oscillator. Turninglike patterns could be produced by each of the following modifications of the model: 1) unilateral descending input and relatively strong reciprocal coupling; 2) unilateral descending input that phase shifted as well as increased the amplitude of the waveform generated by an oscillator on one side; and 3) brief descending modulatory inputs that excited the oscillator on one side and inhibited the contralateral oscillator. In all three cases, there was an increase in “burst” duration ipsilateral to the excitatory input and an increase in cycle time, similar to turning locomotor activity in whole animals. It is likely that turning maneuvers are mediated by descending modulatory inputs primarily to the spinal oscillator networks, which control the timing of burst activity, but perhaps also to motoneurons for axial musculature.