Movements and Muscle Activity Initiated by Brain Locomotor Areas in Semi-Intact Preparations From Larval Lamprey

Abstract

In in vitro brain/spinal cord preparations from larval lamprey, locomotor-like ventral root burst activity can be initiated by pharmacological (i.e., "chemical") microstimulation in several brain areas: rostrolateral rhombencephalon (RLR); dorsolateral mesencephalon (DLM); ventromedial diencephalon (VMD); and reticular nuclei. However, the quality and symmetry of rhythmic movements that would result from this in vitro burst activity have not been investigated in detail. In the present study, pharmacological microstimulation was applied to the above brain locomotor areas in semi-intact preparations from larval lamprey. First, bilateral pharmacological microstimulation in the VMD, DLM, or RLR initiated symmetrical swimming movements and coordinated muscle burst activity that were virtually identical to those during free swimming in whole animals. Unilateral microstimulation in these brain areas usually elicited asymmetrical undulatory movements. Second, with synaptic transmission blocked in the brain, bilateral pharmacological microstimulation in parts of the anterior (ARRN), middle (MRRN), or posterior (PRRN) rhombencephalic reticular nucleus also initiated symmetrical swimming movements and muscle burst activity. Stimulation in effective sites in the ARRN or PRRN initiated higher-frequency locomotor movements than stimulation in effective sites in the MRRN. Unilateral stimulation in reticular nuclei elicited asymmetrical rhythmic undulations or uncoordinated movements. The present study is the first to demonstrate in the lamprey that stimulation in higher-order locomotor areas (RLR, VMD, DLM) or reticular nuclei initiates and sustains symmetrical, well-coordinated locomotor movements and muscle activity. Finally, bilateral stimulation was a more physiologically realistic test of the function of these brain areas than unilateral stimulation.

The Transformation of a Unilateral Locomotor Command into a Symmetrical Bilateral Activation in the Brainstem

“…The importance of a bilaterally symmetrical input to RS cells is further stressed by the need for stimulating RS cells on both sides to elicit symmetrical locomotion. For instance, a unilateral chemical stimulation of reticular nuclei elicits asymmetrical undulations or uncoordinated movements in semi-intact preparations from larval lampreys, whereas bilateral stimulation elicited symmetrical swimming (Jackson et al, 2007). A bilateral symmetrical activation of RS cells is thus important for symmetrical locomotion but unlikely to be the sole contributor.…”

Spinal Cord Injury Induces Changes in Electrophysiological Properties and Ion Channel Expression of Reticulospinal Neurons in Larval Lamprey

“…In larval lamprey, reticulospinal (RS) neurons are both sufficient and necessary for initiation of locomotion (Paggett et al, 2004;Jackson et al, 2007). After a rostral spinal cord transection, axotomized RS neurons regenerate their axons for progressively greater distances caudal to the lesion with increasing recovery times (Davis and McClellan, 1994a,b), and there is a gradual recovery of locomotor function (Davis et al, 1993;McClellan, 1994) (for review, see McClellan, 1998).…”

Descending brain neurons in larval lamprey: Spinal projection patterns and initiation of locomotion

“…Fourth, although part of the PLV extends into the very rostral spinal cord (Fig. 1B), stimulation lateral to the PRRN, in the region of the PLV, does not initiate spinal locomotor activity (Paggett et al, 2004; Jackson et al, 2007). Fifth, activation of trigeminal afferents can initiate locomotor behavior (McClellan, 1984), and some of these afferents project their axons to the very rostral spinal cord (Calton et al, 1998) and potentially might activate spinal CPGs.…”

“…Spinal locomotor activity was initiated by bilaterally symmetrical pharmacological microstimulation in one of several brain locomotor areas, as previously described in detail (Jackson et al, 2005, 2007; see Fig. 1 in Paggett et al 2004): ventromedial diencephalon (VMD); dorsolateral mesencephalon (DLM); or rostrolateral rhombencephalon (RLR).…”

“…In adult and larval lamprey, the lateral spinal tracts are important for the descending initiation of locomotion (McClellan, 1988; also see Ullen et al, 1997). In addition, sustained pharmacological stimulation in reticular nuclei initiates and drives swimming movements and locomotor activity in semi-intact larval lamprey preparations (Jackson et al, 2007). …”