Prey avoidance learning and neuronal elements mediating behavioral switching in the predatory sea-slug Pleurobranchaea californica

Animals decide on appropriate behaviors when encountering various stimuli by integrating sensory information, learning and motivational state. This study takes a neuroethological approach in investigating how the predatory sea-slug Pleurobranchaea californica makes behavioral choices. Pleurobranchaea is a predatory generalist that surveys its environment for potential prey in a trial-and-error fashion. When encountering the Nudibranch Flabellina iodinea and its noxious defense mechanism, the predator quickly learns to avoid the prey and retains the aversive association for up to 72 hours post-training. The conditioning paradigm is highly specific and does not affect the internal state of the animal. Feeding thresholds for the appetitive stimulus betaine are not significantly changed, and it continues to attack a related prey species, Hermissenda crassicornis. This prey avoidance paradigm resembles a situation the predators may face in their natural environments, and it shows how they may make appropriate decisions when choosing suitable prey. After prey avoidance conditioning, feeding on Flabellina is suppressed in trained animals. The activity of identified feeding command neurons (PCP), necessary and sufficient to activate feeding, was examined in whole animal preparations of conditioned and control animals to assay for neural correlates of conditioning. Suppression of PCP activity was consistent in all preparations during presentation of either Flabellina or Hermissenda, but not during presentation of strong appetitive stimuli such as betaine or squid homogenate. This is not consistent with the results observed in intact animals and in previous food aversion paradigms where suppression of feeding was only present in trained animals during presentation of the conditioned stimuli (Davis and Gillette 1978; Davis et al. 1980; Mpitsos and Cohan 1986c). This suggests another source of inhibition, possibly a pain induced effect of surgery. Whole animal preparations exhibited increased feeding thresholds, consistent with a general suppression of feeding. Additionally, pain or distress caused by surgery may cause animals to enter a defensive protective state conserving energy and avoiding contact with natural prey. These results suggest that injury-induced suppression of feeding masks the cellular correlates of prey avoidance learning. In Pleurobranchaea, active feeding and avoidance turning are mutually exclusive behaviors. The decision to exhibit either behavior is made through integrating sensory stimuli and internal state. The neuronal elements mediating this decision were investigated in isolated nervous system preparations. I monitored components of the feeding network, the PCP command neurons and the presynaptic inhibitory interneurons (I2s), during stimulation of the Large Oral Veil Nerve (LOVN) to induce withdrawal and fictive avoidance turning. PCP and I2 activity was inhibited during the withdrawal period (first 5-10 sec post-stimulation) and persisted well into the fictive avoidance turn (the following 30-40 sec). The inhibition of PCP s and I2s was coincident and thus resembled effects of suppression of feeding during the escape swim. It basically differed from learned food avoidance, in which I2s were tonically active during tonic inhibition of PCPs. Members of the swim network were surveyed to determine the source of inhibition. One swim output neuron, Aci-1, that was previously found to strongly inhibit PCP s and I2s via activation of the interneuron I1 during the swim episode, was shown to be similarly activated in a tonic fashion during withdrawal and the avoidance turn. These results thus provide a neuronal correlate to suppression of feeding during avoidance turning