Research Interests

 

The main research interests of the lab are in mechanisms of sensory processing and its plasticity and in animal communication. The two topics are intricately linked, in nature and in our research, because for most sensory systems the processing of communication signals is one of the most important tasks.

Sensory Processing

All information about the environment and our body reaches us through our senses. The sensory filtering mechanisms have been tuned by evolution to efficiently extract behaviourally relevant information from the constant stream of sensory input. The processing of this information by our brain is highly dynamic, it constantly adapts to changing environmental conditions, and it varies with our behavioural state, such as our level of alertness or the behavioural context. To understand how sensory processing and its plasticity work, it is therefore essential to study sensory processing using stimulation conditions as they occur under real-life conditions in the animals’ natural habitat. My research takes this approach using the electrosensory system of weakly electric fish as a model.

Evolution of multiple topographic maps in the brain: Topographic maps are found in most sensory systems. Prominent examples are the retinotopic maps found in visual cortex, the somatotopic maps in the somatosensory system, the computational maps of auditory space described in the midbrain of barn owls, and also the recently described maps of polarization angles in the central complex of locusts. Most systems even contain multiple topographic maps, which may be arranged in parallel, hierarchical, or in a mixed fashion. What distinguishes the processing properties of neurons in different maps of a given system is still poorly understood and difficult to address in systems with complex lateral and hierarchical connectivity. The electrosensory system of weakly electric fish offers a unique window into the neural mechanisms that can differentiate multiple topographic representations, because it contains three somatotopic maps of the body surface that are arranged strictly in parallel. These maps receive identical input from primary electrosensory afferents, but that filter this information in different ways. We investigate the spatial and temporal filtering properties of the three maps using electrophysiological, pharmacological, molecular biological, and computer-modeling approaches.

Related publications:

  • Toscano Márquez B, Dunn RJ, Krahe R (2013) Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish, Apteronotus leptorhynchus. J Comp Neurol 521:1054–1072
  • Krahe R, Bastian J, Chacron MJ (2008) Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 100:852-867
  • Krahe R, Kreiman G, Gabbiani F, Koch C, Metzner W (2002) Stimulus encoding and feature extraction by multiple sensory neurons. J Neurosci 22: 2374-2382

Plasticity of sensory processing:


Sensory processing constantly adapts to changing conditions in the environment (e.g., changing light intensity) and to changes in behavioural condition (e.g., foraging versus communication, sleep versus being awake). Key players in adjusting neural processing properties are feedback loops and neuromodulators. The neuromodulators acetylcholine and serotonin have been implicated in mechanisms of attention, learning and memory, and enhanced processing of sensory stimuli as well as in debilitating diseases such as schizophrenia and depression. In order to fully understand the role of a modulating agent such as acetylcholine in the functioning of the brain, it is essential to directly link specific mechanisms of action at the cellular level to well-described changes in neuronal information transmission and to their role in behaviourally relevant situations. We are investigating the mechanisms by which acetylcholine and serotonin modulate sensory processing as well as their behavioural context in the electrosensory system of weakly electric fish. We combine a range of molecular, electrophysiological, and pharmacological approaches with computer modeling to establish direct links between the action of acetylcholine and serotonin at the cellular and circuit level with the behavioural contexts that activate these systems. This work is conducted in collaboration with Dr. Maurice Chacron, Dept. Physiology, McGill University.

Related publications:

  • Toscano Márquez B, Dunn RJ, Krahe R (2013) Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish, Apteronotus leptorhynchus. J Comp Neurol 521:1054–1072
  • Mehaffey WH, Ellis LD, Krahe R, Dunn RJ, Chacron MJ (2008) Ionic and neuromodulatory regulation of burst discharge controls frequency tuning. J Physiol (Paris) 102:195-208
  • Ellis LD, Krahe R, Bourque CW, Dunn RJ, Chacron MJ (2007) Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. J Neurophysiol 98:1526-1537

Reliability of sensory information transmission: The behaviour of many animals indicates a high precision in the processing of sensory information, which often seems at odds with the large variability of neuronal responses observed during electrophysiological experiments. We have been investigating the potential contributions to the behavioural precision of temporal integration and parallel processing using the electrosensory system of weakly electric fish and the auditory system of grasshoppers as model systems.

Related publications:

  • Savard M, Krahe R, Chacron MJ (2011) Neural heterogeneities influence envelope and temporal coding at the sensory periphery. Neuroscience 172:270-284
  • Ávila-?kerberg O, Krahe R, Chacron MJ (2010) Neural heterogeneities and stimulus properties affect burst coding in vivo. Neuroscience 168:300-313
  • Krahe R, Kreiman G, Gabbiani F, Koch C, Metzner W (2002) Stimulus encoding and feature extraction by multiple sensory neurons. J Neurosci 22: 2374-2382
  • Kreiman G, Krahe R, Metzner W, Koch C, Gabbiani F (2000) Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electric fish Eigenmannia. J Neurophysiol 84:189-204
  • Ronacher B, Krahe R (2000) Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects. Eur J Neurosci 12:2147-2156.

Animal Communication

Communication signals evolve under a range of selection pressures. These include energetic constraints, to be conspicuous for the intended receiver, and not to be conspicuous for unintended receivers such as predators. Sexual selection has a strong shaping influence on mate-attraction and courtship signals. We have been using two approaches to investigating the evolution of communication signals, and we recently added a third:

  1. Behavioural experiments: We have performed behavioural experiments to investigate the recognition and discrimination of communication signals, and we have used mate-preference tests in the laboratory to test whether female weakly electric fish show a preference for certain males based on characteristics of their electric communication signals.

  2. Electrophysiological experiments: The sensory abilities of animals may be one of the drivers of signal evolution. For example, for a male grasshopper to be perceived by a receptive female and to outcompete other males, the animal should generate communication signals that strongly activate the sensory mechanisms of the female. We therefore investigate the sensory mechanisms of signal recognition and of signal discrimination (given that there is a choice of male signals).

  3. Field studies: Some of the limitations of laboratory studies of behaviour are that the animals may not show their full repertoire of natural behaviour and that the properties of their communication signals may be affected by holding conditions in the laboratory. For example, fish may grow much faster and become bigger under laboratory conditions than they would in the wild, because the effort of foraging may be much reduced. Signal properties that might be related to male quality (“good genes”) in the natural habitat may lose this relationship in the laboratory. It is therefore essential to study the characteristics of communication signals and their distribution in natural populations. To this end, we recently started field work on apteronotid electric fish in Peru.

Related publications:

  • Cuddy M, Aubin-Horth N, Krahe R (2012) Electrocommunication behaviour and non-invasively-measured androgen changes following induced seasonal breeding in the weakly electric fish, Apteronotus leptorhynchus. Horm Behav 61:4-11
  • Reardon EE, Parisi A, Krahe R, Chapman LJ (2011) Energetic constraints on electric signalling in wave-type weakly electric fishes. J Exp Biol 214:4141-4150
  • Van der Sluijs I, Gray SM, Amorim MCP, Barber I, Candolin U, Hendry AP, Krahe R, Maan ME, Utne-Palm AC, Wagner H-J, Wong BBM (2011) Communication in troubled waters: Responses of fish communication systems to changing environments. Evol Ecol 25:623–640
  • Fugère V, Ortega H, Krahe R (2011) Electrical signalling of dominance in a wild population of electric fish. Biol Lett 7:197-200
  • Fugère V, Krahe R (2010) Electric signals and species recognition in the wave-type gymnotiform fish, Apteronotus leptorhynchus. J Exp Biol 213:225-236
  • Stamper S, Carrera-G E, Tan EW, Fugère V, Krahe R, Fortune ES (2010) Species differences in group size and electrosensory interference in weakly electric fishes: Implications for electrosensory processing. Behav Brain Res 207:368-376
  • Ronacher B, Wohlgemuth S, Vogel A, Krahe R (2008) Temporal integration and discrimination of acoustic communication signals. J Comp Psychol 122:252-263
  • Krahe R, Budinger E, Ronacher B (2002) Coding of sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition. J Comp Physiol A 187:977-985
  • Ronacher B, Krahe R (2000) Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects. Eur J Neurosci 12:2147-2156.
  • Ronacher B, Krahe R, Hennig RM (2000) Effects of signal duration on the recognition of masked communication signals by the grasshopper Chorthippus biguttulus. J Comp Physiol A 186:1065-1072.
  • Ronacher B, Krahe R (1998) Song recognition in the grasshopper Chorthippus biguttulus is not impaired by shortening song signals: implications for neuronal encoding. J Comp Physiol A 183:729-735.

Collaborations

Cholinergic and serotonergic modulation of sensory processing:
  Dr. Maurice Chacron
Dept. Physiology, McGill University

Communication and speciation of weakly electric fish:
  Dr. Eldredge Birmingham
Smithsonian Tropical Research Institute, Panama City, Republic of Panama
  Dr. Jan Benda
Dept. Biologie II, Ludwig-Maximilians-Universität München, Germany
  Dr. Eric Fortune
New Jersey Institute of Technology, Newark, NJ
  Dr. Hernán Ortega Torres
Departamento de Ictiología, Museo de Historia Natural, Lima, Perú
 
Energetics and hormonal control of electric signaling:
  Dr. Lauren Chapman
Dept. Biology, McGill University
  Dr. Nadia Aubin-Horth
Dept. de Biologie, Université Laval, Québec

 


Funding:

CFI
Canada Foundation for Innovation
NSERC
Natural Sciences and Engineering Research Council of Canada
FQRNT
Fonds de Recherche sur la nature et les technologies

 


Last update: Feb. 12, 2013
 
Field Research
Olivia Bargelletti and Rudiger Krahe measure interindividual distances in a natural population of Sternarchorhynchus spec. in the Rio Llullapichis in Peru (June 2008).
Sketch of the topographic representations of the electrosensory body surface in the hindbrain of A. leptorhynchus (horizontal section). Three maps CMS, CLS, LS) receive identical sensory input from the skin. The fourth map (MS) is part of a second, ampullary electrosensory system.
Short section of a recording of the electric organ discharge (EOD) of Sternarchorhynchus sp.. [To hear an acoustic playback of the EOD, click on the image.]
Recording of the EOD of an Eigenmannia sp..
EOD of a Sternopygus macrurus, a wave-type gymnotiform fish recorded in Peru.
Recording of the EOD of a pulse-type weakly electric fish (Gymnotus sp.)
When disturbed, some pulse-type weakly electric fish display a novelty response, i.e., a transient increase in their discharge rate.
Recording of the EOD of Rhamphichtys sp., a pulse-type gymnotiform fish from Peru.