Dr. Jens Herberholz
University of Maryland

Research(-> home)


Overview

Publications

Projects

Open Positions



crayfishWelcome to the Laboratory of

Crustacean 
Neurobiology &
Behavior




Overview



Research in my lab investigates the neural basis of animal behavior:

We are interested in identifying and examining neural circuitry that underlies offensive and defensive aggression as well as decision-making and behavioral choice
.


We use crayfish as our primary animal model because they display easily quantifiable behavioral patterns, and they feature a nervous system of tractable complexity that is accessible for a variety of neurophysiological and neuropharmacological studies.

Two crayfish fightingMost social animals compete aggressively for resources such as food, shelter and mates. The early stages of an encounter between well-matched crayfish are marked by an aggressive escalation that can include strikes, aggressive posture, grappling with claws, and bouts of offensive tail-flips (Herberholz et al. 2001, Edwards & Herberholz 2005). At some point, fighting in crayfish is interrupted by an abrupt change in the agonistic behavior of one animal as it switches from aggressive to submissive behaviors. This switch marks the change in the dominance status of the animals and identifies the new subordinates (Herberholz et al. 2001). Dominant and subordinate crayfish then show clear differences in their behavior. The dominant animal displays a dominant posture, initiates approaches and attacks, constructs a shelter and claims first access to most resources, while the subordinate displays a submissive posture, retreats and escapes from the dominant, and is left to claim unwanted resources (Herberholz et al. 2001, Edwards et al. 2003, Herberholz et al. 2003, Song et al. 2006, Herberholz et al. 2007). 

dominanceRecently, we found that the stability of dominance relationships is context-dependent. A small change in the social environment, i.e. the presence of another crayfish, quickly disrupts dominance relationships and facilitates reversals of social status (Graham & Herberholz 2009).

In our attempt to understand the behavioral mechanisms underlying social dominance, we use video analysis to identify aggressive and submissive behaviors that are expressed during agonistic interactions in pairs and groups of crayfish. We combine this with non-invasive electrophysiology, intracellular electrophysiology and neuropharmacology to investigate the neural circuitry responsible for dominant and subordinate status.


When attacked by a natural predator (e.g., dragonfly
nymphs), juvenile crayfish produce three different forms of escape tail-flips controlled by as many neural circuits (Herberholz et al. 2004a).
nymph attack
n1  n2 n4   n5
  
Two of the tail-flips are mediated by giant neurons (medial giant and lateral giant) that evoke stereotyped, reflexive escape responses away from the stimulus. One is mediated by non-giant circuitry that produces tail-flips of less stereotyped forms with longer response latencies. The neural circuits that control the tail-flip behavior are only partially understood (Herberholz et al. 2002, Antonsen et al. 2005, Herberholz 2009). We are interested in how the different escape circuits integrate sensory signals and how they interact with each other to produce effective behavioral outputs (Liu & Herberholz 2010). 

We are also interested in decisions-making processes that take place in the nervous system and lead to adaptive behavioral choices. By combining video- and electrophysiological recordings, we can measure behavioral and neural responses to simulated predatory attacks. We expose juvenile crayfish to moving shadows while the animals are searching for food. In response to approaching shadows, each crayfish produces one of two discrete behavioral outputs: it either tail-flips backwards by rapid flexion of its abdomen or it immediately stops forward locomotion and freezes in place (Liden & Herberholz 2008).

shadow response

By using a non-invasive technique to record neural activity (Herberholz et al. 2001, Herberholz et al. 2004a, Herberholz 2009) we are able to identify the underlying neural circuitry that controls the tail-flips produced in response to shadows. When exposed to different predator (shadow) signals combined with food incentives of different qualities, crayfish make suprisingly complex decisions by carefully balancing risk against potential gain; this identifies crayfish as a new and important model to study value-based decision making (Liden et al. 2010). The different components of the circuitry are accessible for intracellular electrophysiology, and we are planning to test the effects of neuromodulators on these circuits. In addition, we are currently investigating how internal states of the animals (e.g., social, motivational, and developmental) affect the decisions that lead to discrete behavioral choices. 

To identify discrete patterns of neural activity that are correlated with status-related behaviors and decision-making, we use manganese-enhanced Magnetic Resonance Imaging (MEMRI).MEMRI

brainManganese, a paramagnetic contrast agent and calcium analog, can highlight active brain areas. Preliminary experiments with live crayfish have shown that they are well suited for MEMRI studies because they have no blood-brain barrier and can easily be restrained within the imaging apparatus. Crayfish tolerate long imaging sessions in high magnetic fields, and they can be placed in small imaging coils which results in images of very high spatial resolution. We have previously demonstrated the feasibility of MEMRI for identification and reconstruction of neural structures in crayfish; thus, manganese can be used as a contrast agent for crayfish neural tissue (Herberholz et al. 2004b). Recently we found that MEMRI can also be used to visualize functional uptake of manganese into brain areas of live juvenile crayfish. Stimulation of one of the animals' antennae led to localized unilateral labeling in areas of the brain that received input from the stimulated antenna. This shows that MEMRI has the potential to allow identification of stimulus-evoked neural activity in live animals at near single-cell resolution (Herberholz et al. 2011).





   

Publications
  1. Herberholz J., Mishra S.H., Uma D., Germann M.W., Edwards D.H., and Potter K. (2011) Non-invasive imaging of neuroanatomical structures and neural activation with high-resolution MRI. Frontiers in Behavioral Neuroscience 5:16. doi: 10.3389/fnbeh.2011.00016. 
  2. Liden W.H., M.L. Phillips and J. Herberholz (2010) Neural control of behavioural choice in juvenile crayfish. Proceedings of the Royal Society B 277: 3493-3500. 
  3. Liu Y.C. and J. Herberholz (2010) Sensory activation and receptive field organization of the lateral giant escape neurons in crayfish. Journal of Neurophysiology 104: 675-684.
  4. Herberholz J. (2009) Recordings of neural circuit activation in freely behaving animals. The Journal of Visualized Experiments 29: http://www.jove.com/index/details.stp?id=1297
  5. Graham M.E. and J. Herberholz (2009) Stability of dominance relationships in crayfish depends on social context. Animal Behaviour 77: 195-199.
  6. Liden W.H. and J. Herberholz (2008) Behavioral and neural responses of juvenile crayfish to moving shadows. The Journal of Experimental Biology 211: 1355-1361.
  7. Herberholz J., C. McCurdy and D.H. Edwards (2007) Direct benefits of social dominance in juvenile crayfish. The Biological Bulletin 213: 21-27.
  8. Herberholz J. (2007) The neural basis of communication in crustaceans. In: Evolutionary ecology of social and sexual systems: crustaceans as model organisms, J. E. Duffy and M. Thiel (eds). Oxford University Press: 71-89.
  9. Song C.-K., J. Herberholz and D.H. Edwards (2006) The effects of social experience on the behavioral response to unexpected touch in crayfish. The Journal of Experimental Biology 209: 1355-1363.
  10. Edwards D.H. and J. Herberholz (2005) Crustacean models of aggression. In: The Biology of Aggression, R. J. Nelson (ed). Oxford University Press: 38-61
  11. Antonsen B.L., J. Herberholz and D.H. Edwards (2005) The retrograde spread of synaptic potentials and recruitment of presynaptic inputs. The Journal of Neuroscience 25 (12): 3086-3094
  12. Herberholz J., C.J. Mims, X. Zhang, X. Hu and D.H. Edwards (2004) Anatomy of a live invertebrate revealed by manganese-enhanced Magnetic Resonance Imaging. The Journal of Experimental Biology 207: 4543-4550
  13. Herberholz J., M.M. Sen and D.H. Edwards (2004) Escape behavior and escape circuit activation in juvenile crayfish during prey-predator interactions. The Journal of Experimental Biology 207: 1855-1863
  14. Edwards D.H., F.A. Issa and J. Herberholz (2003) The neural basis of dominance hierarchy formation in crayfish. Microscopy Research and Technique 60: 369-376
  15. Herberholz J., M.M. Sen and D.H. Edwards (2003) Parallel changes in agonistic and non-agonistic behaviors during dominance hierarchy formation in crayfish. The Journal of Comparative Physiology A 189: 321-325
  16. Herberholz J., B.L. Antonsen and D.H. Edwards (2002) A lateral excitatory network in the escape circuit of crayfish. The Journal of Neuroscience 22 (20): 9078-9085 
  17. Drummond J., F.A. Issa, C.K. Song, J. Herberholz, S.R. Yeh and D.H. Edwards (2002) Neural mechanisms of dominance hierarchies in crayfish. In: The Crustacean Nervous System, K. Wiese (ed).  Springer Verlag, Berlin: 124-135
  18. Herberholz, J. and B. Schmitz (2001) Signaling via water currents in behavioral interactions of snapping shrimp (Alpheus heterochaelis). The Biological Bulletin 201 (1): 6-16
  19. Herberholz J., F.A. Issa and D.H. Edwards (2001) Patterns of neural circuit activation and behavior during dominance hierarchy formation in freely behaving crayfish. The Journal of Neuroscience 21 (8): 2759-2767
  20. Edwards D.H., B.L. Antonsen and J. Herberholz (2001) Network, neuronal and biochemical computations in the escape circuit of crayfish. In: Proceedings of the Eleventh Yale Workshop on Adaptive and Learning Systems, K. S. Narendra (ed). Center for Systems Science, Yale University, New Haven: 225-232
  21. Herberholz J. and B. Schmitz (1999) Flow visualisation and high speed video analysis of water jets in the snapping shrimp (Alpheus heterochaelis). The Journal of Comparative Physiology A 185: 41-49
  22. Herberholz J. and B. Schmitz (1998) Role of mechanosensory stimuli in intraspecific agonistic encounters in the snapping shrimp (Alpheus heterochaelis). The Biological Bulletin 195 (2): 156-167
  23. Schmitz B. and J. Herberholz (1998) Snapping behaviour in intraspecific agonistic encounters in the snapping shrimp (Alpheus heterochaelis). The Journal of Biosciences 23 (5): 623-632

     click here for a complete list of publications including conference proceedings and theses (pdf) 




   

Projects
 

Current projects investigate :

        1. Mechanisms underlying decision-making and behavioral choice 

           2. Mechanisms underlying formation and maintenance of dominance relationships

           3. Neural circuit organization & multi-sensory integration

   


  
 

Open Positions 


Freshmen and sophomores can participate as a Maryland Student Researcher in the Maryland Center for Undergraduate Research (http://www.ugresearch.umd.edu/programs.html).
 

Students participating in this program work individually with faculty members and earn a citation on their transcript for participation in the program.

Junior and seniors can earn academic credit for research participation (maximum of 9 credits) through PSYC479 or BSCI399.
 


I am currently on sabbatical leave and will accept students again for the fall semester 2012!




last modified: 12-22-2011; copyright by Jens Herberholz 2005