The purpose of the present study was to determine the numbers of descending brainstem projections to different levels of the spinal cord in normal larval sea lamprey (Petromyzon marinus) and to examine the restoration of these projections in animals 3-32 weeks after transection of the rostral spinal cord (approximately 10% of body length). In normal animals approximately 1,250, 900, and 825 brainstem neurons projected to 20%, 40%, and 60% of body length, respectively. Spinal projections originated from the diencephalon, mesencephalon, three rhombencephalic reticular nuclei, Müller and Mauthner neurons, and four cell groups in the caudal rhombencephalon. In spinal cord-transected animals the number of brainstem neurons projecting to 20% of body length increased with recovery time, and at 32 weeks post-transection the total number and distribution of brainstem neurons was not significantly different from normal animals. Brainstem projections first appeared at 40% of body length by 8 weeks post-transection, and were present at 60% of body length by 32 weeks post-transection. There was substantial restoration of brainstem projections to 40% of body length but limited restoration to 60% of body length. The approximately 50 brainstem neurons, including some Müller cells, that projected to 60% of body length at 32 weeks post-transection indicate that restoration of descending projections in excess of 50 mm can occur within the central nervous system of this vertebrate. These anatomical results are discussed in relation to the time course of recovery of locomotor function in spinal cord-transected lampreys.

1. Receptor blockers for inhibitory amino acids were applied to part or all of the spinal cord of larval lamprey during brain stem-initiated locomotor activity. Blocking glycinergic inhibition with strychnine applied to the entire spinal cord converted the locomotor pattern from left-right alternation to synchronous left-right bursting. The results suggest that left and right oscillators are connected by relatively strong reciprocal inhibitory (glycinergic) connections in parallel with weaker reciprocal excitatory connections. This possible organization was supported by results from a computer model consisting of left and right oscillators connected by reciprocal inhibition and excitation in parallel. In addition, the results suggest that reciprocal inhibition is not required for left-right rhythmicity but rather is involved primarily with phasing of left-right activity. 2. Locally blocking glycinergic inhibition with strychnine in the rostral spinal cord resulted in synchronous left-right burst activity in that region of the cord as well as in more caudal areas of the cord in which reciprocal inhibition should still be functional. 3. Blocking glycinergic inhibition in the caudal spinal cord converted the pattern in that region of the cord to left-right synchronous activity. The effects in the ascending direction on the burst patterns in more rostral areas of the spinal cord were less than those mentioned above in the descending direction with application of strychnine to the rostral spinal cord. 4. With glycinergic inhibition or GABAergic inhibition blocked in the entire spinal cord, stable longitudinal coupling along the spinal cord persisted. This and the neurophysiology results mentioned above suggest that the main mechanism for longitudinal coupling between locomotor networks in adjacent regions of the spinal cord is ipsilateral excitatory connections and not crossed inhibitory connections. This possible organization was supported by results from a computer model, which consisted of a pair of oscillators in the more rostral and more caudal spinal cord that could be connected by various types of coupling schemes. 5. The neurophysiological data above suggest that ipsilateral, excitatory coupling is stronger in the descending direction than in the ascending direction. In the computer model, a dominant descending coupling is a necessary requirement to produce positive longitudinal phase lags.

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In larval lamprey, hemitransections were performed on the right side of the rostral spinal cord to axotomize ipsilateral reticulospinal (RS) neurons. First, at short recovery times (2-3 weeks), uninjured RS neurons contralateral to hemitransections fired a smooth train of action potentials in response to sustained depolarization, whereas axotomized neurons fired a single short burst or short repetitive bursts. For uninjured RS neurons, the afterpotentials of action potentials had three components: fast afterhyperpolarization (fAHP), afterdepolarizing potential (ADP), and slow AHP (sAHP) that was attributable to calcium influx via high-voltage-activated (HVA) (N-and P/Q-type) calcium channels and calcium-activated potassium channels (SKKCa). For axotomized RS neurons, the fAHP was significantly larger than for uninjured neurons, and the ADP and sAHP were absent or significantly reduced. Second, at relatively long recovery times (12-16 weeks), axotomized RS neurons displayed firing patterns and afterpotentials that were similar to those of uninjured neurons. Third, mRNA levels of lamprey HVA calcium and SKKCa channels in axotomized RS neurons were significantly reduced at short recovery times and restored at long recovery times. Fourth, blocking calcium channels in uninjured RS neurons resulted in altered firing patterns that resembled those produced by axotomy. We demonstrated previously that lamprey RS neurons in culture extend neurites, and calcium influx results in inhibition of neurite outgrowth or retraction. Together, these results suggest that the downregulation of Ca 2ϩ channels in axotomized RS neurons, and the associated reduction in calcium influx, maintain intracellular calcium levels in a range that is permissive for axonal regeneration.

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