Physiological basis of feeding behavior in Tritonia diomedea. II. Neuronal mechanisms.
1. The nudibranch mollusk Tritonia diomedea feeds by biting and drawing pieces of coelenterate sea whips into its buccal cavity. It then swallows them in a series of cyclic ingestion movements. The coordinated pattern of swallowing can be elicited in reduced preparations by stimulation of identifiable neurons in cerebral or buccal ganglia. 2. Swallowing normally proceeds as a cyclic pattern of protraction and retraction movements driven by alternating bursts in odontophore-radula protractor and retractor motor neurons (MNs), with simultaneous coordination of many other major neurons. 3. Brief or prolonged constant-current stimulation of certain individual buccal ganglion (SW) premotor neurons reliably triggers one or more complete cycles of impulse bursts in motor neurons with coordinated movements of the jaws and buccal mass. The MN bursts produced in this way resemble the ones seen during feeding. Some SW neurons trigger responses that greatly exceed the duration of the stimulus; others drive cyclic output in the motor system whose duration corresponds closely to the duration of the depolarizing current. As well, the rate of MN bursting can be modulated by steady currents of different amplitudes injected into these SW neurons. There are, however, alternative sensory and motor routes independent of SW neurons by which the motor pattern may be elicited and modulated. 4. A search for the source of the feeding rhythm resulted in the identification of a pair of motor neurons (B5) that have prominent burst and pattern-generating capabilities independent of SW activation. They fire vigorous impulse bursts on rebound from spontaneously occurring IPSP waves or from imposed hyperpolarizing potentials of similar amplitude and duration. 5. Constant prolonged depolarizing currents injected into B5 result in the production of repetitive bursts in other MNs that resemble in amplitude and time course those seen during feeding. Cyclic bursting generated in this way apparently entrains other parts of the feeding motor generator since a coordinated output of appropriately phased hyperpolarizing waves, antagonistic EPSP volleys, motor bursts, and movements is simultaneously recorded in other, unstimulated motor neurons of the system. However, the SW neurons are not always entrained by such MN-generated bursting. 6. Brief stimulation of B5 (sufficient to elicit one or a few impulses) also results in the appearance of a depolarizing afterpotential, which is itself capable of regenerating further impulses. When prolonged, constant currents are applied, the impulses that result form bursts whose durations and interburst intervals depend on the amplitude of the stimulating currents. The spike and burst-generating qualities of these neurons (which may include endogenous and interactive components) are sufficient to serve as a source of timing and phasing for the motor pattern.
D000818:Animals; D004594:Electrophysiology; D005247:Feeding Behavior / Q000502:physiology*; D005724:Ganglia / Q000166:cytology / Q000502:physiology*; D066298:In Vitro Techniques; D007395:Interneurons / Q000502:physiology; D008974:Mollusca / Q000502:physiology*; D009046:Motor Neurons / Q000502:physiology; D009433:Neural Inhibition; D009435:Synaptic Transmission