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Sound Localization L24. Mate Calling in Animal Communication Crickets: a model system for studies of neuroethology of rhythmic behavior Oct. 5, 2011 BioNB 4240 Cornell University BioNB424 Neuroethology 1 2 © Carl D. Hopkins Why Study Animal Communication Signals? Why Invertebrates? Why Insects? Why Crickets? 1) Readily accessible nervous systems 1) The signals (=Displays) tend to be “Fixed” Action Patterns (FAPs) - all-or-none, highly stereotyped - large cells (because they need to be redundant and quickly recognized) - small number of cells often released by social stimuli; signals also act as releasers - cells may be consistently identified in each individual 2) Complexity vs. Tractability 2) Relatively simple behavior - Am. Comm. signals are interesting (more complex than most - more reliable than many vertebrates FAPs) - stereotyped: reliable and repeatable. - greater stereotypy than many vertebrate signals 3) Ubiquity and Functionality - nearly all animals communicate - adaptive significance of signals can be readily assessed 4) Sensory, Motor, and Sensory-Motor Integration 3 4 3 Different Song Types Calling Acheta domesticus Gryllus rubens Songs Chirps 1) Calling song is for 5 advertisement 0 Trill 2) Aggression song 10 kHz occurs when a Allonemobius sparsalus Oecanthus californicus male enters another male‟s territory and a fight ensues 3) Courtship song 0 Hz occurs when a Eunemobius confusus Gryllotalpa major female enters a male‟s territory in response to his call 2 sec 5 T. Walker Singing crickets of North America 6 http://buzz.ifas.ufl.edu/index.htm 1 Acheta domesticus Teleogryllus texensis Divergence between the Courtship Songs of the Field Crickets Gryllus texensis and Gryllus rubens (Orthoptera, Gryllidae) Mark J. Fitzpatrick & David A. Gray Ethology Volume 107 Issue 12 Page 1075-1085, December 2001 7 8 Song Variation Song Variation Pulses Pulses - number of cycles - number of cycles - duration - duration - carrier frequency - carrier frequency Chirps/Trills Chirps/Trills - number of pulses - number of pulses - duration - duration - pulse period (rate) - pulse period (rate) - inter-pulse interval - inter-pulse interval Chirp Rates Chirp Rates 9 10 What Song Features Matter to Females? Sound Production 1) Females prefer a narrow range of pulse rates 2) Preference matches pulse rates of conspecific song F M 11 12 Gryllus wings are sexually dimorphic 2 Sounds are Generated 1) The right wing lays with the Forewings over the left wing (Tegmen; ; tegmina) 2) As the wings close, the plectrum of the left wing scrapes The plectrum serves as a against the file of the scraper, which rubs against right wing the file of the opposite wing 3) Each notch in the file corresponds to a single cycle within the The harp serves as a pulse resonator that amplifies the sound at the carrier 4) Full closure of the frequency wings corresponds to a single pulse 5) No sound on opening 13 14 H. Bennett-Clark. J. Exp. Biol. 206:1479. 15 16 Gryllus campestris close Neuromuscular Sound Calling Activity During open Songs Closer Song Production Opener Gryllus bimaculatus -Studies of David close open Bentley closer -Wings opened with depressor muscles opener (M99) - Wings closed with Gryllus campestris elevator muscles Courtship (M90) Songs - Pulse characteristics determined by MUSCLE Gryllus bimaculatus CONTRACTION and WING MORPHOLOGY 17 18 3 Songs can be triggered or Stimulating at different inhibited by stimulating in frequencies has direct certain parts of the brain effects on chirping or in the connectives frequency, but no effects going from the brain to the on characteristics of thoracic ganglia pulses or chirps Stimulation Stimulation Frequency This suggests that song This suggests that chirp production is INITIATED characteristics are IN THE BRAIN CONTROLLED BY THE GANGLIA 19 20 Hierarchical Song Control Central Pattern Generators (CPG) 1) Neural circuits that drive stereotyped, programmed, rhythmic 3) Sound Familiar? movements 4) Unlike original FAP concept, 2) Activation results in output patterns are not completely fixed output patterns in stereotyped. Different patterns the absence of can be produced through continued input or neuromodulatory inputs feedback 5) Generally a result of both cellular Chirp Decision Chirp Parameters Pulse Parameters (pulse (ion channels) and network (yes/no, chirp rate) (pulse rate, number duration, number of cycles, properties of pulses, chirp carrier frequency) duration) 21 22 Central Pattern Ion Channel Central Pattern Post-Inhibitory Generators (CPG) Properties Generators (CPG) Rebound Rhythmic Burster Pacemaker Inhibitory Input No Post-Inhibitory Rebound Post-Inhibitory Rebound 1) Resting Potential > Threshold Hyperpolarization-activated Na+ channels 2) Ca2+-activated K+ Channels 23 24 4 Central Pattern Post-Inhibitory Rebound Central Pattern Generators (CPG) plus Generators (CPG) Reciprocal Inhibition Dep Open Wing Motor Neuron Start Elev + - To Depressor Sound - + End Rhythmic Activity in Rate of cycling can determine + Phase with Song, To Elevator the pulse rate within chirps - Alternating with Interneuron Inhibition Close Wing 25 26 Central Pattern Central Pattern Generators (CPG) Generators (CPG) Interneurons that There are interneurons in the ganglia that are rhythmically active in show rhythmic phase with chirps: they most likely start and stop the cycling of pulses excitation within chirps, determining pulse number and chirp duration Interneurons that show rhythmic inhibition at the same time This can explain pulse rate, but CPG must also control pulse number/chirp duration 27 28 Command Neurons Identification of the (Kupferman and Weiss 1978) Cricket Song Command Neuron (Hedwig 1996, 2000) Criteria for Designation as a „Command Neuron‟: 1) Correlation: Neuron‟s activity should be directly related to production of the behavior 2) Sufficiency: Stimulating neuron should induce behavior 3) Necessity: Inhibiting neuron should eliminate behavior 29 30 5 Identification of the Cricket Song Command Neuron (Hedwig 1996, 2000) Command neuron stimulation. 31 32 The criteria of both necessity and Genetics of sufficiency have been Cricket Song met. Thus, it is likely the (Bentley and Hoy, 1972; command neuron that Hoy et al. 1977) drives chirping. Hybrids have calls that As predicted, command are intermediate in neuron activity only several features influences chirp Females prefer the calls production. It has NO of their hybrid crosses EFFECT on pulses within chirp, which are Calls and preferences controlled by the CPG in are genetically the meta- and meso- controlled and thoracic ganglia correlated 33 34 Review of Important General Concepts Evolution of a silent crickets on Kauai 1) Sound production involves interactions between peripheral sound- generating structures and central nervous system control of those structures 2) Sound motor output is hierarchically organized. Decision command pattern generation muscle contraction 3) Stereotyped motor output is often under the control of central pattern generators (CPGs) that operate in the absence of any additional input. (CPG is a cellular/circuit oscillator) 4) CPGs may be activated by „command neurons‟, which are defined as both necessary and sufficient for production of the behavior 5) Vocal communication signals may be genetically controlled and tightly linked to the genetics of the auditory system. 6) Cricket sound production is advantageous for communication (but vulnerable to parasitism). Zuk, M., Rotenberry, J. T., and Tinghitella, R. M. (2006). Silent night: adaptive disappearance of a sexual35 36 signal in a parasitized population of field crickets. Biology Letters. DOI:10.1098/rsbl.2006.0539 6 .
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