SUMMARY The neural systems that control escape behavior have been studied intensively in several animals, including mollusks, fish and crayfish. Surprisingly little is known, however, about the activation and the utilization of escape circuits during prey–predator interactions. To complement the physiological and anatomical studies with a necessary behavioral equivalent, we investigated encounters between juvenile crayfish and large dragonfly nymphs in freely behaving animals using a combination of high-speed video-recordings and measurements of electric field potentials. During attacks, dragonfly nymphs rapidly extended their labium, equipped with short, sharp palps, to capture small crayfish. Crayfish responded to the tactile stimulus by activating neural escape circuits to generate tail-flips directed away from the predator. Tail-flips were the sole defense mechanism in response to an attack and every single strike was answered by tail-flip escape behavior. Crayfish used all three known types of escape tail-flips during the interactions with the dragonfly nymphs. Tail-flips generated by activity in the giant neurons were predominantly observed to trigger the initial escape responses to an attack, but non-giant mediated tail-flips were often generated to attempt escape after capture. Attacks to the front of the crayfish triggered tail-flips mediated either by the medial giant neuron or by non-giant circuitry, whereas attacks to the rear always elicited tail-flips mediated by the lateral giant neuron. Overall, tail flipping was found to be a successful behavior in preventing predation, and only a small percentage of crayfish were killed and consumed.
A phasic stimulus directed to the rear of a crayfish (Procambarus clarkii) creates mechanosensory input to the lateral giant (LG) interneuron, a command neuron for escape. A single LG spike is necessary and sufficient to produce a highly stereotyped tail flip that thrusts the animal away from the source of stimulation. Here we describe a lateral excitatory network among primary afferent axons in the last abdominal ganglion of crayfish that produces nonlinear amplification of the sensory input to the command circuitry for escape. The lateral excitation is mediated by electrical synapses between central terminals of primary mechanosensory afferents. The network enables stimulated afferents to recruit unstimulated afferents that contribute additional input to LG and to mechanosensory interneurons that also converge on LG. When depolarized, the LG neuron increases its own inputs from primary afferents and primary interneurons by facilitating the recruitment of both. Conversely, hyperpolarization of LG reduces the excitability of primary afferents and primary interneurons. The crayfish's decision to escape, previously thought to lie exclusively in the synaptic integrative properties of LG, is now seen to depend on the interactions between LG dendritic postsynaptic potentials and the responses of primary afferent terminals in the lateral excitatory network.
Crayfish are known for their innate aggressiveness and willingness to quickly establish dominance relationships among group members. Consequently, the formation of dominance hierarchies and the analysis of behavioral patterns displayed during agonistic encounters have mostly been tested in environments that provide no immediate resources besides space. We tested the hypothesis that social hierarchy formation in crayfish serves to determine access to future resources. Individuals within groups of three juvenile crayfish were allowed to form a social hierarchy in a featureless environment before a single food resource was presented. Higher dominance indices were significantly correlated with increased access to the food. The highest ranked crayfish spent more time in contact with the food than did medium-ranked and lowest ranked crayfish, and crayfish of medium rank spent more time in contact with the resource than did lowest ranked animals. The highest ranked crayfish consolidated their dominant status in the presence of food, indicated by a complete absence of any submissive behaviors during that period. The results of these experiments show that the disposition of crayfish to engage in fighting and formation of a dominance hierarchy in a featureless environment serves to determine future access to an emerging resource, thereby entailing greater benefits for animals of higher social rank.
One of the most important decisions animals have to make is how to respond to an attack from a potential predator. The response must be prompt and appropriate to ensure survival. Invertebrates have been important models in studying the underlying neurobiology of the escape response due to their accessible nervous systems and easily quantifiable behavioral output. Moreover, invertebrates provide opportunities for investigating these processes at a level of analysis not available in most other organisms. Recently, there has been a renewed focus in understanding how value-based calculations are made on the level of the nervous system, i.e., when decisions are made under conflicting circumstances, and the most desirable choice must be selected by weighing the costs and benefits for each behavioral choice. This article reviews samples from the current literature on anti-predator decision making in invertebrates, from single neurons to complex behaviors. Recent progress in understanding the mechanisms underlying value-based behavioral decisions is also discussed.
Creation of a dominance hierarchy within a population of animals typically involves a period of agonistic activity in which winning and losing decide relative positions in the hierarchy. Among crayfish, fighting between size-matched animals leads to an abrupt change of behavior as the new subordinate retreats and escapes from the attacks and approaches of the dominant (Issa et al., 1999). We used high-speed videography and electrical recordings of aquarium field potentials to monitor the release of aggressive and defensive behavior, including the activation of neural circuits for four different tail-flip behaviors. We found that the sequence of tail-flip circuit excitation traced the development of their dominance hierarchy. Offensive tail flipping, attacks, and approaches by both animals were followed by a sharp rise in the frequency of nongiant and medial giant escape tail flips and a fall in the frequency of offensive tail flips of the new subordinate. These changes suggest that sudden, coordinated changes in the excitability of a set of neural circuits in one animal produce the changes in behavior that mark its transition to subordinate status.
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