For twenty years, our lab has worked with crayfish to study how social experience shapes the nervous system and behavior. Much of this research involves the analysis of two prominent neural circuits that control rapid escape movements. Crayfish engage these circuits to escape from danger directed to the front by activating the medial giant neurons (MGs), or when attacked from the rear, the lateral giant neurons (LGs). We aim to better understand how social experiences modulate the two giant fiber circuits that control these tail-flip behaviors, and you can read further about the lab’s contributions to the history of these circuits in a recent review published in Frontiers in Physiology.
The lab’s work includes investigations into a variety of topic areas, including:
- the gut-brain axis
- sensitivity to acute alcohol exposure
- economic decision-making
- social dominance hierarchies
Gut-brain axis
For the past few years, one focus of the lab’s work has revolved around studies of the gut-brain axis.
This work originated in a project supported by NSF from 2019 to 2024. The lab collaborated with the Bentley, Ghodssi, and Losert labs to investigate the complex effects of intestinal serotonin on both gut and brain health, developing a realistic picture of the gut-microbiome-brain axis system. This work appears across a pair of papers published in Microsystems & Nanoengineering (https://doi.org/10.1038/s41378-020-00208-z; https://doi.org/10.1038/s41378-020-00184-4). Our lab has also worked with the Ghodssi lab to engineer a bioelectronic device to understand the co-modulation of dopamine and serotonin: an in vivo application that simultaneously monitors both dopamine and serotonin in real-time in freely behaving crayfish underwater. That paper was published in ACS Sensors (https://doi.org/10.1021/acssensors.3c02304). Most recently, in collaboration with the Losert lab, we investigated the role of the central nervous system as well as serotonergic modulation on hindgut motility (https://royalsocietypublishing.org/doi/full/10.1098/rsos.250094).
In addition, funded by a BSOS Dean’s Research Initiative, we work together with the Maisel lab to investigate the relationship between social experience and permeability of the gut epithelium (‘leaky gut”) in crayfish. Our lab has also been collaborating with the Burgess and Hall labs to identify the connections between social experience and gut microbiota.
Alcohol
A significant focus of the lab has been on revealing the effects of social experience on behavioral and neural responses to acute alcohol exposure.
Funded by the National Institute on Alcohol Abuse and Alcoholism, we have shown that both juvenile and adult crayfish are behaviorally sensitive to alcohol (ethanol; EtOH), and this sensitivity is affected by the prior social experience of the animals. Compared to socially isolated crayfish, crayfish taken from a communal tank (“group-housed”) exhibit higher behavioral sensitivity to EtOH. In addition, we found that the differences in EtOH sensitivity are paralleled on the level of single neurons (the LG and MG neurons). The first paper on this topic was published in the Journal of Experimental Biology (https://doi.org/10.1242/jeb.154419). Our lab has subsequently uncovered that social isolation causes a change in the expression of specific receptors in the crayfish giant circuits, including those that are targeted by alcohol. This work appeared in Frontiers in Physiology (https://doi.org/10.3389/fphys.2018.00448) and the Journal of Neurophysiology (https://doi.org/10.1152/jn.00519.2020).
Peptide & metabolite identification
Led by the Nemes lab and in collaboration with the Araneda, Cao, El-Sayed, Quinlan, and Speer labs, this project uses extraction of cytoplasm from a single giant neuron in crayfish. Cytoplasmic samples will be analyzed with ultra-high mass spectroscopy in the Nemes lab to identify changes in gap junction proteins to see how electrical neurotransmission is modulated over time and life stages.
Crayfish are central to the project due to their identified giant (LG/MG) neurons that are embedded in a circuit rich in electrical synapses. This allows us to advance the technology of proteome collection and processing with reduced peptide losses compared to currently available methods, a central focus of the project.
Decision-making
Historically, our lab has investigated economic decision-making, and this work has influenced questions and methods across more recent work on alcohol and the gut-brain axis.
Fueled by funding from the National Science Foundation, we studied the behavioral and neural basis of anti-predator behavior in crayfish. One of the most important decisions all organisms have to make is how to respond to a life-threatening event. In the case of crayfish, these decisions are made quickly and the underlying neurobiology can be investigated (https://doi.org/10.1242/jeb.010165). Crayfish that are searching for food make discrete and easily quantifiable choices when exposed to simulated predator attacks, they either freeze or swim away (‘tail-flip”), and their decisions are controlled by nerve cells (MG neurons) that are large, identifiable, and accessible. Interestingly, the lab discovered that crayfish make economic decisions, adjusting their ratios of freezing and tail-flipping according to a cost-benefit analysis (https://royalsocietypublishing.org/doi/full/10.1098/rspb.2010.1000). If the food quality is high, crayfish predominately freeze, which is risky but keeps them close to the expected food reward. Hungry animals also default to freezing because this behavioral choice is of higher value compared to tail-flipping, which increases distance between the animal and its next meal (https://link.springer.com/article/10.1007/s00359-017-1158-8). Furthermore, after social isolation, crayfish produce more MG-mediated tail-flips (and fewer freezes) compared to socially-experienced animals, suggesting that isolation can lead to maladaptive behavior by increasing threat sensitivity (https://doi.org/10.1242/jeb.226704)
Social Dominance
Crayfish form social hierarchies through aggressive dyadic interactions, and once dominance relationships have been established, they typically remain stable. We have shown that these social dominance relationships can also be transient. They can be disrupted with the brief defeat of the dominant by a larger animal (https://doi.org/10.1016/j.anbehav.2008.09.027) so long as the subordinate is present when the defeat takes place—and it must, in fact, witness the dominants defeat to successfully reverse its social status (https://doi.org/10.1086/BBLv230n2p152).
We also found that prior social experience affects individual responses in subsequent fights. When we compared crayfish that were housed in pairs for one week and free to exchange sensory signals to those that were completely isolated from each other and deprived of sensory communication, agonistic (aggressive and submissive) behaviors increased in subsequent fights after total isolation. In animals that exchanged sensory cues in-between fights, the modality of the sensory signal mattered for subsequent agonistic behavior. Prior olfactory communication led to an increase in aggression and disrupted dominance relationships in subsequent fights, whereas the prior exchange of visual cues reduced aggression and rank reversals, suggesting that the effect of these signals on shared neural circuitry is context dependent (https://doi.org/10.1242/jeb.226704).