Swimming rhythm in decerebrated, paralyzed stingrays: normal and abnormal coupling

Abstract

Rhythmic motoneuronal activity was recorded from decerebrated, paralyzed stingrays and compared with electromyograms recorded from the same animals. Before and after paralysis, a rostral-to-caudal sequence of alternation occurred between dorsal (elevator) and ventral (depressor) efferents. The swimming pattern was thus observed in the absence of phasic afferent input, and this constitutes fictive locomotion. After paralysis, both the intersegmental delay (time between activation at progressively caudal recording sites) and the burst duration remained linearly related to the swim cycle period. In many instances, neither the slope nor the intercept was significantly altered by immobilization. The intercepts all fell near the origin, indicating that the fictive rhythm remains constant phase coupled. Although the swimming rhythm was obtained after paralysis, some differences occurred. These included fewer and shorter spontaneous sequences, a greater range of cycle periods, and longer burst durations. During fictive swimming, the burst duration:cycle period ratio usually increased to 0.53 from 0.39 observed before paralysis. Therefore, the silent periods seen between burst discharges in antagonist efferents during movement were often absent after paralysis. Mechanical stimulation of the tail reduced both cycle periods and burst durations; however, the burst:cycle ratio remained greater than or equal to 0.50. The linear relation between burst duration and cycle period found for spontaneous sequences was not changed by stimulation of the tail. During fictive swimming the inter- and intrasegmental coupling that characterizes stingray swimming becomes labile. Abnormal coupling appears more often during sequences with long swim cycles. Intrasegmental coupling is tighter than intersegmental coupling at any cycle period. Rhythmic activity at one segmental level can be independent of activity at other levels. This suggests that multiple oscillator circuits exist that are not dependent on propriospinal circuits interconnecting different segments. Rhythmicity in elevator and depressor motoneurons is not dependent on reciprocal connections between the circuitry driving the motor nuclei. Therefore, separate oscillators for elevators and depressors appear to be present within one spinal segment.

Locomotion evoked by stimulation of the brain stem in the Atlantic stingray, Dasyatis sabina

“…The brain was exposed from the spinomedullary junction to the caudal boundary of the telencephalon. The animals were anemically decerebrated (Droge and Leonard, 1983a) and the cerebellum removed. The brain was transected at the caudal boundary of the midbrain.…”

“…As an alternative to studying locomotion in preparations in which the motor pattern is as complex as that in cats or as simple as that in lampreys, Leonard and colleagues developed the Atlantic stingray, Dasyatis sabina, as a model for vertebrate locomotion (Coggeshall et al, 1978;Leonard et al, 1979;Williams et al, 198 1;Droge and Leonard, 1983a, b). Previously in the stingray, we identified the ventral half of the lateral funiculus as the locus of the primary pathway for the initiation of locomotion; a second pathway was identified in the dorsolateral funiculus (DLF) (Williams et al, 1984).…”

Neuroecology of cartilaginous fishes: the functional implications of brain scaling

“…The lateral portion of the tegmentum receives input from the spinal cord (Hayle, 1973) and tectum (Boord & Northcutt, 1982; Smeets et al , 1983) and the lateral mesencephalic complex is the site for termination of secondary electrosensory, mechanosensory and auditory fibres (Boord & Northcutt, 1982; Corwin & Northcutt, 1982). Cell groups in this area have been identified, including the midbrain reticular formation, which plays an important role in controlled locomotion in chondrichthyans (Demski, 1977; Droge & Leonard, 1983 a,b ), as observed in mammals (Mori et al , 1980) and teleosts (Kashin et al , 1974).…”

Multielectrode analysis of coordinated, multisite, rhythmic bursting in cultured CNS monolayer networks

“…6). It is interesting that the cycle periods of rhythms generated by intact spinal cords are often considerably increased when phasic afferent feedback is removed pharmacologically (Droge and Leonard, 1983). It is also interesting that small, monolayer networks in culture (300-500 neurons) can generate alternating activity, which is a basic feature of rhythms observed in intact spinal cords.…”

“…scratching rhythms can persist after the spinal cord is isolated from descending and peripheral influences (Grillner and Wallen, 1985;Stein and Grossman, 1980) local circuits must exist that are capable of pattern generation. Consequently, there has been a trend toward further simplification of vertebrate preparations both surgically and pharmacologically (Cohen and Harris-Warrick, 1984;Droge and Leonard, 1983;Grillner and Wallen, 1985;Grillner et al, 1983;McClellan and Farel, 1985;Roberts et al, 1981;Stein and Grossman, 1980). Despite considerable progress, these preparations still retain an enormous complexity that limits the identification of cellular components involved in rhythmic pattern generation.…”