Roles of ascending inhibition during two rhythmic motor patterns in Xenopus tadpoles.
We have investigated the effects of ascending inhibitory pathways on two centrally generated rhythmic motor patterns in a simple vertebrate model, the young Xenopus tadpole. Tadpoles swim when touched, but when grasped respond with slower, stronger struggling movements during which the longitudinal pattern of motor activity is reversed. Surgical spinal cord transection to remove all ascending connections originating caudal to the transection (in tadpoles immobilized in alpha-bungarotoxin) did not affect "fictive" swimming generated more rostrally. In contrast, cycle period and burst duration both significantly increased during fictive struggling. Increases were progressively larger with more rostral transection. Blocking caudal activity with the anesthetic MS222 (pharmacological transection) produced equivalent but reversible effects. Reducing crossed-ascending inhibition selectively, either by midsagittal spinal cord division or rostral cord hemisection (1-sided transection) mimicked the effects of transection. Like transection, both operations increased cycle period and burst duration during struggling but did not affect swimming. The changes during struggling were larger with more rostral hemisection. Reducing crossed-ascending inhibition by spinal hemisection also increased the rostrocaudal longitudinal delay during swimming, and the caudorostral delay during struggling. Weakening inhibition globally with low concentrations of the glycine antagonist strychnine (10-100 nM) did not alter swimming cycle period, burst duration, or longitudinal delay. However, strychnine at 10-60 nM decreased cycle period during struggling. It also increased burst duration in some cases, although burst duration increased as a proportion of cycle period in all cases. Strychnine reduced longitudinal delay during struggling, making rostral and caudal activity more synchronous. At 100 nM, struggling was totally disrupted. By combining our results with a detailed knowledge of tadpole spinal cord anatomy, we conclude that inhibition mediated by the crossed-ascending axons of characterized, glycinergic, commissural interneurons has a major influence on the struggling motor pattern compared with swimming. We suggest that this difference is a consequence of the larger, reversed longitudinal delay and the extended burst duration during struggling compared with swimming.
Green
C S
CS
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, United Kingdom.
Soffe
S R
SR
D000344:Afferent Pathways / Q000503:physiopathology; D062365:Aminobenzoates / Q000494:pharmacology; D000777:Anesthetics / Q000494:pharmacology; D000818:Animals; D002038:Bungarotoxins / Q000494:pharmacology; D002818:Cordotomy; D004924:Escape Reaction / Q000187:drug effects / Q000502:physiology*; D005998:Glycine / Q000037:antagonists & inhibitors / Q000502:physiology; D018684:Glycine Agents / Q000494:pharmacology; D007814:Larva; D009043:Motor Activity / Q000187:drug effects / Q000502:physiology*; D009498:Neurotoxins / Q000494:pharmacology; D010507:Periodicity; D013116:Spinal Cord / Q000503:physiopathology*; D013119:Spinal Cord Injuries / Q000503:physiopathology; D013331:Strychnine / Q000494:pharmacology; D013550:Swimming / Q000502:physiology; D014982:Xenopus laevis / Q000254:growth & development / Q000502:physiology*
D062365:Aminobenzoates; D000777:Anesthetics; D002038:Bungarotoxins; D018684:Glycine Agents; D009498:Neurotoxins; C003636:tricaine; D013331:Strychnine; D005998:Glycine