Associative olfactory learning in the desert locust, Schistocerca gregaria

SUMMARY Locusts can learn associations between olfactory stimuli and food rewards, and use the acquired memories to choose between foods according to their nutrient requirements. They are a model system for both the study of olfactory coding and insect nutritional regulation. Previous studies have used operant paradigms for conditioning freely moving locusts, restricting the study of the neural mechanisms underlying the acquisition of olfactory memories, which requires restrained preparations for electrophysiological recordings. Here we present two complementary paradigms for the classical conditioning of olfactory memories in restrained desert locusts (Schistocerca gregaria). These paradigms allow precise experimental control over the parameters influencing learning. The first paradigm is based on classical (Pavlovian) appetitive conditioning. We show that opening of the maxillary palps can be used as a measure of memory acquisition. Maxillary palp opening in response to odour presentation is significantly higher in locusts trained with paired presentation of an odour and a food reward than in locusts trained either with unpaired presentation of food and odour or the odour alone. The memory formed by this conditioning paradigm lasts for at least 24 h. In the second paradigm, we show that classical conditioning of an odour memory in restrained locusts influences their decisions in a subsequent operant task. When locusts that have been trained to associate an odour with a food reward are placed in a Y-maze, they choose the arm containing that odour significantly more often than naïve locusts. A single conditioning trial is sufficient to induce a significant bias for that odour for up to 4 h. Multiple- and block-trial training induce a significant bias that lasts at least 24 h. Thus, locusts are capable of forming appetitive olfactory memories in classical conditioning paradigms and can use these memories to modify their decisions.

[1]  J. Dubnau,et al.  Deconstructing Memory in Drosophila , 2005, Current Biology.

[2]  Daniel R. Papaj,et al.  Insect learning: ecological and evolutionary perspectives. , 1992 .

[3]  Formation of long term olfactory memory in honeybees does not require protein synthesis , 1993, Naturwissenschaften.

[4]  V. Rehder Quantification of the honeybee's proboscis reflex by electromyographic recordings , 1987 .

[5]  M. Srinivasan,et al.  The concepts of ‘sameness’ and ‘difference’ in an insect , 2001, Nature.

[6]  David Raubenheimer,et al.  The Hungry Locust , 2000 .

[7]  David F. Sherry,et al.  Interval Timing by an Invertebrate, the Bumble Bee Bombus impatiens , 2006, Current Biology.

[8]  R. Menzel Memory dynamics in the honeybee , 1999, Journal of Comparative Physiology A.

[9]  R. Chapman,et al.  The importance of palpation in food selection by a polyphagous grasshopper (Orthoptera: Acrididae) , 2005, Journal of Insect Behavior.

[10]  M. Dicke,et al.  Olfactory learning by predatory arthropods , 2006 .

[11]  Frederic Mery,et al.  A Cost of Long-Term Memory in Drosophila , 2005, Science.

[12]  D. Raubenheimer,et al.  Associative learning by locusts: pairing of visual cues with consumption of protein and carbohydrate , 1997, Animal Behaviour.

[13]  D. Laloi,et al.  Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure , 2000, Animal Behaviour.

[14]  T. Carew,et al.  Invertebrate learning and memory: from behavior to molecules. , 1986, Annual review of neuroscience.

[15]  Daniel R. Papaj,et al.  ECOLOGICAL AND EVOLUTIONARY ASPECTS OF LEARNING IN PHYTOPHAGOUS INSECTS , 1989 .

[16]  J. Dubnau,et al.  13 Memories of Worms and Flies: From Gene to Behavior , 2007 .

[17]  M. Mizunami,et al.  Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning , 2006, The European journal of neuroscience.

[18]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[19]  Alex Kacelnik,et al.  State-Dependent Learned Valuation Drives Choice in an Invertebrate , 2006, Science.

[20]  Anderson,et al.  Behavioural analysis of olfactory conditioning in the moth spodoptera littoralis (Boisd.) (Lepidoptera: noctuidae) , 1997, The Journal of experimental biology.

[21]  M. Mizunami,et al.  Olfactory Learning and Memory in the Cockroach Periplaneta americana , 2001 .

[22]  W. Quinn,et al.  Classical conditioning and retention in normal and mutantDrosophila melanogaster , 1985, Journal of Comparative Physiology A.

[23]  D. Laloi,et al.  Prior classical olfactory conditioning improves odour-cued flight orientation of honey bees in a wind tunnel , 2005, Journal of Experimental Biology.

[24]  D. Raubenheimer,et al.  Locusts learn to associate visual stimuli with drinking , 1994, Journal of Insect Behavior.

[25]  S. Behmer Insect herbivore nutrient regulation. , 2009, Annual review of entomology.

[26]  K. Daly,et al.  Associative olfactory learning in the moth Manduca sexta. , 2000, The Journal of experimental biology.

[27]  M. Mizunami,et al.  Temporal determinants of long-term retention of olfactory memory in the cricket Gryllus bimaculatus. , 2002, The Journal of experimental biology.

[28]  S. Behmer,et al.  Variable rewards and discrimination ability in an insect herbivore: what and how does a hungry locust learn? , 2005, Journal of Experimental Biology.

[29]  Patrizia d'Ettorre,et al.  Associative learning in ants: conditioning of the maxilla-labium extension response in Camponotus aethiops. , 2010, Journal of insect physiology.

[30]  M. Mizunami,et al.  Olfactory learning in the cricket Gryllus bimaculatus. , 2000, The Journal of experimental biology.

[31]  J. Niven,et al.  Are Bigger Brains Better? , 2009, Current Biology.

[32]  N. Balderrama One trial learning in the American cockroach, Periplaneta americana , 1980 .

[33]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[34]  E. Bernays,et al.  A study of behavioural habituation to a feeding deterrent in nymphs of Schistocerca gregaria , 1984 .

[35]  E. Bernays Aversion Learning and Feeding , 1993 .

[36]  N. Koeniger The biology of the honey bee , 1988, Insectes Sociaux.

[37]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[38]  M. Mizunami,et al.  Lifetime olfactory memory in the cricket Gryllus bimaculatus , 2002, Journal of Comparative Physiology A.

[39]  R. F. Chapman,et al.  THE FUNCTIONS OF THE MAXILLARY PALPS OF ACRIDIDAE (ORTHOPTERA) , 1970 .

[40]  S. J. Simpson,et al.  A comparison of dietary selection behaviour in larval Locusta migratoria and Spodoptera littoralis , 1988 .

[41]  R. Dukas,et al.  Learning improves growth rate in grasshoppers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Menzel,et al.  Effects of two bitter substances on olfactory conditioning in the moth Heliothis virescens , 2007, Journal of Experimental Biology.

[43]  D. Laloi,et al.  Olfactory conditioning of the proboscis extension in bumble bees , 1999 .

[44]  E. Bernays,et al.  Food tastes and toxic effects: associative learning by the polyphagous grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae) , 1990, Animal Behaviour.

[45]  R. Dukas Evolutionary biology of insect learning. , 2008, Annual review of entomology.

[46]  Thomas Preat,et al.  Olfactory conditioning of proboscis activity in Drosophila melanogaster , 2006, Journal of Comparative Physiology A.

[47]  S. J. Simpson,et al.  Associative learning and locust feeding: evidence for a ‘learned hunger’ for protein , 1990, Animal Behaviour.

[48]  Locusts show rapid individual learning but no social learning about food , 2009, Animal Behaviour.

[49]  E. Bernays,et al.  Food aversion learning in the polyphagous grasshopper Schistocerca americana , 1988 .

[50]  E. Bernays,et al.  Post-ingestive feedbacks and associative learning regulate the intake of unsuitable sterols in a generalist grasshopper. , 1999, The Journal of experimental biology.