Responses of reticulospinal neurons in intact lamprey to pitch tilt

Abstract

In the swimming lamprey, a postural control system maintains a definite orientation of the animal's longitudinal axis in relation to the horizon (pitch angle). Operation of this system is based on vestibular reflexes. Important elements of the postural network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections from the brain stem to the spinal cord. Here we describe responses to vestibular stimulation (rotation of the animal in the pitch plane) in RS neurons of intact lampreys. The activity of neurons was recorded from their axons in the spinal cord by chronically implanted arrays of macroelectrodes. From the multielectrode recordings of mass activity, discharges in individual axons were extracted by means of a spike-sorting program, and the axon position in the spinal cord and its conduction velocity were determined. Vestibular stimulation was performed by rotating the animal in steps of 45 degrees throughout 360 degrees or by periodical "trapezoid" tilts between the nose-up and -down positions. Typically, the RS neurons exhibited both dynamic responses (activity during movement) and static responses (activity in a new sustained position). The neurons were classified into two groups according to their pattern of response. Group UP neurons responded preferentially to nose-up rotation with maximal activity at 0-135 degrees up. Group DOWN neurons responded preferentially to nose-down rotation with maximal activity at 0-135 degrees down. Neurons of the two groups also differed in the position of their axons in the spinal cord and axonal conduction velocity. An increase in water temperature, which presumably causes a downward turn in swimming lampreys, affected the activity in the UP and DOWN groups differently, so that the ratio UP responses to DOWN responses increased. We suggest that the UP and DOWN groups mediate the opposing vestibular reflexes and cause the downward and upward turns of the animal, respectively. The lamprey will stabilize the orientation in the pitch plane at which the effects of UP and DOWN groups are equal to each other. In addition to the main test (rotation in the pitch plane), the animals were also tested by rotation in the transverse (roll) plane. It was found that 22% of RS neurons responding to pitch tilts also responded to roll tilts. The overlap between the pitch and roll populations suggests that the RS pathways are partly shared by the pitch and roll control systems.