The effects of alcohol on society can be devastating, both as an immediate consequence of acute intoxication and as a powerful drug of abuse. However, the neurocellular mechanisms of alcohol intoxication are still elusive, partly because of the complex interactions between alcohol and nervous system function. We found that juvenile crayfish are behaviorally sensitive to acute alcohol exposure and progress through stages that are strikingly similar to those of most other intoxicated organisms. Most surprisingly, we found that the social history of the animals significantly modified the acute effects of alcohol. Crayfish taken from a rich social environment became intoxicated more rapidly than animals that were socially isolated before alcohol exposure. In addition, we found that the modulation of intoxicated behaviors by prior social experience was paralleled on the level of individual neurons. These results significantly improve our understanding of the mechanisms underlying the interplay between social experience, alcohol intoxication and nervous system function.

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Crayfish are capable of two rapid, escape reflexes that are mediated by two pairs of giant interneurons, the lateral giants (LG) and the medial giants (MG), which respond to threats presented to the abdomen or head and thorax, respectively. The LG has been the focus of study for many decades and the role of GABAergic inhibition on the escape circuit is well-described. More recently, we demonstrated that the LG circuit is sensitive to the acute effects of ethanol and this sensitivity is likely mediated by interactions between ethanol and the GABAergic system. The MG neurons, however, which receive multi-modal sensory inputs and are located in the brain, have been less studied despite their established importance during many naturally occurring behaviors. Using a combination of electrophysiological and neuropharmacological techniques, we report here that the MG neurons are sensitive to ethanol and experience an increase in amplitudes of post-synaptic potentials following ethanol exposure. Moreover, they are affected by GABAergic mechanisms: the facilitatory effect of acute EtOH can be suppressed by pretreatment with a GABA receptor agonist whereas the inhibitory effects resulting from a GABA agonist can be occluded by ethanol exposure. Together, our findings suggest intriguing neurocellular interactions between alcohol and the crayfish GABAergic system. These results enable further exploration of potentially conserved neurochemical mechanisms underlying the interactions between alcohol and neural circuitry that controls complex behaviors.

Like most social animals, crayfish readily form dominance relationships and linear social hierarchies when competing for limited resources. Competition often entails dyadic aggressive interactions, from which one animal emerges as the dominant and one as the subordinate. Once dominance relationships are formed, they typically remain stable for extended periods of time; thus, access to future resources is divided unequally among conspecifics. We previously showed that firmly established dominance relationships in juvenile crayfish can be disrupted by briefly adding a larger conspecific to the original pair. This finding suggested that the stability of social relationships in crayfish was highly context-dependent and more transient than previously assumed. We now report results that further identify the mechanisms underlying the destabilization of crayfish dominance relationships. We found that rank orders remained stable when conspecifics of smaller or equal size were added to the original pair, suggesting that both dominant and subordinate must be defeated by a larger crayfish in order to destabilize dominance relationships. We also found that dominance relationships remained stable when both members of the original pair were defeated by larger conspecifics in the absence of their original opponent. This showed that dominance relationships are not destabilized unless both animals experience defeat together. Lastly, we found that dominance relationships of pairs were successfully disrupted by larger intruders, although with reduced magnitude, after all chemical cues associated with earlier agonistic experiences were eliminated. These findings provide important new insights into the contextual features that regulate the stability of social dominance relationships in crayfish and probably in other species as well.

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