Activation patterns of embryonic chick lumbosacral motoneurones following large spinal cord reversals.

Abstract

SUMMARY1. Embryonic chick motoneurones were caused to innervate inappropriate hindlimb muscles by rotating the presumptive lumbosacral region of the neural tube in stage 15-16 embryos which is prior to the outgrowth of motoneurone axons.2. The activation patterns of motoneurones in control and spinal cord reversal embryos were analysed from electromyographic (e.m.g.) recordings of stage 36 limb muscles during evoked movement sequences in an isolated spinal cord-limb preparation. Histograms representing the frequency of activation were constructed for each muscle. The muscle's pattern of activation was classified as flexor-like or extensor-like and compared to the activation patterns of control muscles.3. A series of control operations was performed in which the prospective lumbosacral region of the neural tube was removed and replaced in its original orientation. Muscles in these embryos were innervated by their normal motoneurone pools and they were activated normally, indicating that the neural tube operation per se does not alter the activation pattern of motoneurones. Furthermore, some muscles (twelve out of sixty-one) in spinal cord reversal embryos had normal activation patterns and appeared to be innervated by their original motoneurones. Based on these results and the result of a previous study (Landmesser & O 'Donovan, 1984 b), it is concluded that motoneurones in reversed spinal cords are activated in a manner appropriate for their original identity.4. The majority of muscles (thirty-three out of sixty-one) in large spinal cord reversal embryos were activated during an appropriate phase of the kicking cycle.Of the remaining muscles, 16 % were activated inappropriately (i.e. extensor muscles were activated as flexors, and vice versa), and 30 % had a novel 'mixed' flexor-and extensor-like activation pattern. However, the activation pattern of most muscles differed markedly from that of any other control muscles regardless of whether the muscle was activated appropriately or inappropriately as a flexor or extensor. The abnormal activation patterns are a likely consequence of the diffuse distribution of inappropriate motoneurones projecting to foreign muscles in embryos with large spinal cord reversals. Since it is likely that motoneurones are still activated according * Present address:

Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Functional aspects

“…According to the myotypic specification theory of Weiss (1 94 1, 1955), one might expect that the pattern generating circuitry of thoracic spinal cord innervating limb muscles would develop properties resembling those of normal lumbar cord. However, the present results, as well as other related studies (Butler et al, 1986;Straznicky, 1963;Narayanan and Hamburger, 1971;Vogel, 1987;Landmesser and O'Donovan, 1984b), indicate that this is not the case. The EMG pattern of specific hindlimb muscles innervated by thoracic motoneurons closely resembled the patterns normally observed in thoracically-innervated intercostal muscles.…”

Selective Fasciculation and Divergent Pathfinding Decisions of Embryonic Chick Motor Axons Projecting to Fast and Slow Muscle Regions

“…This is supported by the observation that although motoneurons to each of the three muscles tested underwent selective fasciculation and selective targeting, different patterns of activity were shown to occur in the fast and slow regions of only the AITIB and IFIB (see also Landmesser and O'Donovan, 1984a;Vogel, 1987) but not the SART. Nevertheless, electrical activity may still be required for normal projections to develop.…”

“…D, In a different embryo, PITIB axons remained partially sorted in the proximal portion of the muscle nerve (arrow indicates area of axon mixing) but (Figure legend continues) Patterned electrical activity has been shown to be required for the normal segregation of lateral geniculate axons into ocular dominance columns in the visual cortex (for review, see Goodman and Shatz, 1993). Furthermore, previous studies have shown that the anterior and posterior regions of the I FI B have different patterns of activation in an in vitro spinal cord-hindlimb preparation at stage 36 (Landmesser and O'Donovan, 1984a,b;Vogel, 1987). Therefore, we were interested to know whether activity could play a determining role in the segregation of axons into fast and slow fascicles within the muscle nerve or the subsequent innervation of discrete regions of the muscle target.…”

“…This observation together with the lack of molecular markers for young fast and slow motoneurons has led many investigators to favor initial nonselective innervation (for review, see Jolesz and Sreter, 1981). In contrast, the fact that neonatal rodent motor units are strongly biased toward one fiber type (for mouse, see Jansen, 1988, 1990; for rat, see Thompson et al, 1984Thompson et al, , 1987Thompson et al, , 1990; and for rabbit, see Gordon and Van Essen, 1985;Soha et al, 1987;Cramer and Van Essen, 1995) favors selective innervation, as do several other experimental studies in both chick and mammal (Feng et al, 1965;Hnik et al, 1967;Hoh, 1975;Soileau et al, 1987;Vogel, 1987;Vogel and Landmesser, 1987;Rafuse et al, 1996).…”

Hoxc10 and Hoxd10 regulate mouse columnar, divisional and motor pool identity of lumbar motoneurons

“…The aberrant innervation of extensor muscles in the thigh, such as the quadriceps, by motoneurons that normally innervate flexor muscles in WT animals most likely contributed significantly to the locomotor defects in double mutants. If motoneurons receive their usual complement of central connections, as occurs when they innervate inappropriate muscles following surgical manipulations (Landmesser and O'Donovan, 1984;Vogel, 1987), then both extensors and flexors would be activated at the same time, leading to the rigid extended posture of limbs in mutant animals.…”