Maintained function of foreign and appropriate junctions on reinnervated goldfish extraocular muscles

Abstract

1. The ability of a multiply innervated muscle to become dually innervated, that is to accept a functional innervation from both its original and a foreign nerve, was investigated using the superior oblique muscle (s.o. muscle) of the goldfish.2. Dual innervation of s.o. muscles was achieved by allowing the original nerve (cranial NIV) to regenerate to its s.o. muscle which had been previously denervated and cross-innervated by a foreign nerve (cranial NIII), or by allowing the original and the foreign nerve to regenerate simultaneously to a denervated muscle.3. Behavioural observations suggested that in some fish reinnervation of the s.o. muscle by its original nerve repressed the function of a previously established foreign innervation. However, physiological tests which involved the stimulation of both foreign and appropriate nerves, and the recording of mechanical and electrical activity of the s.o. muscle, demonstrated that there was no functional displacement of foreign innervation on these muscles, even on individual dually innervated fibres.4. Dual innervation of the s.o. muscle persisted, apparently unchanged, for as long as the observations were continued (up to 7 months). The s.o. muscle contains two populations of fibres, fast and slow, and both types became and remained dually innervated.5. When both NIII and NIV were allowed to regenerate simultaneously to a denervated s.o. muscle there was no obvious selectivity in the final pattern of innervation. On the average both nerves elicited approximately equal tension from s.o. muscles, and evoked excitatory junctional potentials (e.j.p.s) of similar mean quantal contents.6. ;Myotypic respecification' was shown not to be responsible for the discrepancy between the behavioural results which sugested that repression of foreign innervation had occurred, and the physiological results which demonstrated that this was not the case. Anatomical and physiological findings indicated that the discrepancy was attributable to eye rotation produced by regenerated inferior oblique muscle fibres which contracted simultaneously with the cross-innervated s.o. muscle. The net result was an eye movement in which the activity of the s.o. muscle was masked.7. It is concluded that repression of established foreign neuromuscular connexions following reinnervation by the embryologically correct nerve does not occur on goldfish extraocular muscles. The s.o. muscle can become non-selectively innervated by both foreign and appropriate axons, and remains so, at least for several months.