Neural mechanisms of reward in insects

Annual Review of Entomology

Volumn 58, Issue , 2013, Pages 543-562

  Perry, Clint J ^a   Barron, Andrew B ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

dopamine; learning; octopamine; reinforcement; reward; VUMmx1

Indexed keywords

DOPAMINE; OCTOPAMINE;

ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; HISTOLOGY; INSECT; LEARNING; METABOLISM; MUSHROOM BODY; PHYSIOLOGY; REVIEW; REWARD;

ANIMALS; DOPAMINE; DROSOPHILA MELANOGASTER; INSECTS; LEARNING; MUSHROOM BODIES; OCTOPAMINE; REWARD;

EID: 84873872936     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-120811-153631     Document Type: Review

References (102)

1. Barron AB, Maleszka R, Van Der Meer RK, Robinson GE. 2007. Octopamine modulates honey bee dance behavior. Proc. Natl. Acad. Sci. USA 104:1703-7
2. Barron AB, Robinson GE. 2008. The utility of behavioral models and modules in molecular analyses of social behavior. Genes Brain Behav. 7:257-65
3. Barron AB, Søvik E, Cornish JL. 2010. The roles of dopamine and related compounds in reward-seeking behavior across animal phyla. Front. Behav. Neurosci. 4:163
4. Berridge KC. 2000. Measuring hedonic impacts in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev. 24:173-98
5. Berridge KC. 2007. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 191:391-431
6. Berridge KC, Robinson TE. 1998. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 28:309-69
7. Berridge KC, Robinson TE, Aldridge JW. 2009. Dissecting components of reward: 'liking, ' 'wanting, ' and learning. Curr. Opin. Pharmacol. 9:65-73
8. Berridge KC, Venier IL, Robinson TE. 1989. Taste reactivity analysis of 6-hydroxydopamine-induced aphagia: implications for arousal and anhedonia hypotheses of dopamine function. Behav. Neurosci. 103:36-45
9. Bicker G, Menzel R. 1989. Chemical codes for the control of behaviour in arthropods. Nature 37:33-39
10. Bindra D. 1978. How adaptive behavior is produced: a perceptual- motivational alternative to response reinforcements. Behav. Brain Sci. 1:41-52
11. Bitterman ME, Menzel R, Fietz A, Scḧafer S. 1983. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97:107-19
12. Busch S, Selcho M, Ito K, Tanimoto H. 2009. A map of octopaminergic neurons in the Drosophila brain. J. Comp. Neurol. 513:643-67
13. Busch S, Tanimoto H. 2010. Cellular configuration of single octopamine neurons in Drosophila. J. Comp. Neurol. 518:2355-64
14. Cabanac M. 1992. Pleasure: the common currency. J. Theor. Biol. 155:173-200
15. Christiansen F, Zube C, Andlauer TFM, Wichmann C, Fouquet W, et al. 2011. Presynapses in Kenyon cell dendrites in the mushroom body calyx of Drosophila. J. Neurosci. 31:9696-707
16. Erber J, Kloppenburg P, Scheidler A. 1993. Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073-83
17. Fahrbach SE. 2006. Structure of the mushroom bodies of the insect brain. Annu. Rev. Entomol. 51:209-32
18. Farooqui T, Robinson K, Vaessin H, Smith BH. 2003. Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neurosci. 23:5370-80
19. Farooqui T, Vaessin H, Smith BH. 2004. Octopamine receptors in the honeybee (Apis mellifera) brain and their disruption by RNA-mediated interference. J. Insect Physiol. 50:701-13
20. Farris SM, Robinson GE, Fahrbach SE. 2001. Experience-and age-related outgrowth of the intrinsic neurons in the mushroom bodies of the adult worker honeybee. J. Neurosci. 21:6395-404
21. Fresquet N. 1999. Effects of aging on the acquisition and extinction of excitatory conditioning in Drosophila melanogaster. Physiol. Behav. 67:205-11
22. Galizia CG, Menzel R. 2001. The role of glomeruli in the neural representation of odours: results from optical recording studies. J. Insect Physiol. 47:115-30
23. Gardner EL. 2005. Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol. Biochem. Behav. 81:263-84
24. Giurfa M. 2007. Invertebrate cognition: nonelemental learning beyond simple conditioning. In Invertebrate Neurobiology, ed. G North, RJ Greenspan, pp. 281-308. New York: Cold Spring Harb. Press
25. Hammer M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63
26. Hammer M, Menzel R. 1995. Learning and memory in the honeybee. J. Neurosci. 15:1617-30
27. Hammer M, Menzel R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5:146-56
28. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4:266-75
29. Homberg U, Christensen TA, Hildebrand JG. 1989. Structure and function of the deutocerebrum in insects. Annu. Rev. Entomol. 34:477-501
30. Honjo K, Furukubo-Tokunaga K. 2009. Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. J. Neurosci. 29:852-62
31. Hull CL. 1943. Principles of Behavior: An Introduction to Behavior Theory. New York: Appleton-Century. 422 pp.
32. Kaira SP. 1997. Appetite and body weight regulation: Is it all in the brain? Neuron 19:227-30
33. Kelley AE, Berridge KC. 2002. The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci. 22:3306-11
34. Kim Y-C, Lee H-G, Han K-A. 2007. D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J. Neurosci. 27:7640-47
35. Kranz GS, Kasper S, Lanzenberger R. 2010. Reward and the serotonergic system. Neuroscience 166:1023-35
36. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S. 2009. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416-27
37. Kreissl S, Eichm̈uller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol. 348:583-95
38. Kuwabara M. 1957. Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene Apis mellifera. J. Fac. Sci. Hokkaido Univ. (Ser. 6) 13:458-64
39. Leknes S, Tracey I. 2008. A common neurobiology for pain and pleasure. Nat. Rev. Neurosci. 9:314-20
40. Liu C, Plaçais P-Y, Yamagata N, Pfeiffer BD, Aso Y, et al. 2012. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512-16
41. Loeb J. 1918. Forced Movements, Tropisms and Animal Conduct. New York: Dover. 209 pp.
42. Mahler SV, Smith KS, Berridge KC. 2007. Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances 'liking' of a sweet reward. Neuropsychopharmacology 32:2267-78
43. Menzel R. 2001. Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8:53-62
44. Menzel R, Erber J, Masuhr T, Browne LB. 1974. Learning andMemory in the Honeybee. Berlin: Springer-Verlag. 366 pp.
45. Menzel R, Giurfa M. 2001. Cognitive architecture of a mini-brain: the honeybee. Trends Cogn. Sci. 5:62-71
46. Mercer AR, Menzel R. 1982. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J. Comp. Physiol. A 145:363-68
47. Mizunami M, Unoki S, Mori Y, Hirashima D, Hatano A, Matsumoto Y. 2009. Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biol. 7:46
48. Mobbs PG. 1982. The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos. Trans. R. Soc. Lond. B 298:309-54
49. Monastirioti M. 1999. Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc. Res. Tech. 45:106-21
50. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V. 1995. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J. Comp. Neurol. 356:275-87
51. Monastirioti M, Linn CE, White K. 1996. Characterization of Drosophila tyramine β-hydroxylase gene and isolation of mutant flies lacking octopamine. J. Neurosci. 16:3900-11
52. O'Donnell P. 2003. Dopamine gating of forebrain neural ensembles. Eur. J. Neurosci. 17:429-35
53. Olds J, Milner P. 1954. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 47:419-27
54. Pani L, Gessa GL. 1997. Evolution of the dopaminergic system and its relationships with the psychopathology of pleasure. Int. J. Clin. Pharmacol. Res. 17:55-58
55. Pecina S, Berridge KC. 2005. Hedonic hot spot in nucleus accumbens shell: Where do μ-opioids cause increased hedonic impact of sweetness? J. Neurosci. 25:11777-86
56. Pecina S, Cagniard B, Berridge KC, Aldridge JW, Zhuang XX. 2003. Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards. J. Neurosci. 23:9395-402
57. Pecina S, Schulkin J, Berridge KC. 2006. Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biol. 4:8
58. Pfl̈uger HJ, Stevenson PA. 2005. Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct. Dev. 34:379-96
59. Ranaldi R, Wise RA. 2001. Blockade of D1 dopamine receptors in the ventral tegmental area decreases cocaine reward: possible role for dendritically released dopamine. J. Neurosci. 21:5841-46
60. Rescorla RA. 1988. Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 11:329-52
61. Roeder T. 1999. Octopamine in invertebrates. Prog. Neurobiol. 59:533-61
62. Roitman MF, Stuber GD, Phillips PEM, Wightman RM, Carelli RM. 2004. Dopamine operates as a subsecond modulator of food seeking. J. Neurosci. 24:1265-71
63. Routtenberg A, Lindy J. 1965. Effects of availability of rewarding septal and hypothalamic stimulation on bar pressing for food under conditions of deprivation. J. Comp. Physiol. 60:158-61
64. Scheiner R, Erber J, Page RE. 1999. Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J. Comp. Physiol. A 185:1-10
65. Schroeter U, Malun D, Menzel R. 2007. Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res. 327:647-67
66. Schroll C, Riemensperger T, Bucher D, Ehmer J, V̈oller T, et al. 2006. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16:1741-47
67. Schultz W. 1998. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80:1-27
68. Schultz W. 2002. Getting formal with dopamine and reward. Neuron 36:241-63
69. Schultz W. 2007. Behavioral dopamine signals. Trends Neurosci. 30:203-10
70. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. 2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23:10495-502
71. Selcho M, Pauls D, Han K-A, Stocker RF, Thum AS. 2009. The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS ONE 4:e5897
72. Sinakevitch I, Niwa M, Strausfeld NJ. 2005. Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J. Comp. Neurol. 488:233-54
73. Sitaraman D, Zars M, Zars T. 2010. Place memory formation in Drosophila is independent of proper octopamine signaling. J. Comp. Physiol. A 196:299-305
74. Skinner BF. 1933. The rate of establishment of a discrimination. J. Gen. Psychol. 9:302-50
75. Smith BH, Huerta R, Bazhenov M, Sinakevitch I. 2012. Distributed plasticity for olfactory learning and memory in the honey bee brain. In Honeybee Neurobiology and Behavior, ed. GC Galizia, D Eisenhardt, M Giurfa, pp. 393-409. New York: Springer
76. Smith KS, Berridge KC, Aldridge JW. 2011. Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc. Natl. Acad. Sci. USA 108:E255-64
77. Smith KS, Mahler SV, Peci ̃ na S, Berridge KC. 2010. Hedonic hotspots: generating sensory pleasure in the brain. In Pleasures of the Brain, ed. ML Kringelbach, KC Berridge, pp. 27-49. New York: Oxford Univ. Press
78. Smith KS, Tindell AJ, Aldridge JW, Berridge KC. 2009. Ventral pallidum roles in reward and motivation. Behav. Brain Res. 196:155-67
79. Szechtman H, Hershkowitz M, Simantov R. 1981. Sexual behavior decreases pain sensitivity and stimulated endogenous opioids in male rats. Eur. J. Pharmacol. 70:279-85
80. Takeda K. 1961. Classical conditioned response in the honey bee. J. Insect Physiol. 6:168-79
81. Tanimoto H, Heisenberg M, Gerber B. 2004. Event timing turns punishment into reward. Nature 430:983
82. Tatemoto K, Carlquist M, Mutt V. 1982. Neuropeptide Y-a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659-60
83. Thorndike EL. 1898. Animal Intelligence: An Experimental Study of the Associative Processes in Animals. New York: Macmillan. 109 pp.
84. Thorndike EL. 1933. An Experimental Study of Rewards. New York: Columbia Univ.
85. Thum AS, Jenett A, Ito K, Heisenberg M, Tanimoto H. 2007. Multiple memory traces for olfactory reward learning in Drosophila. J. Neurosci. 27:11132-38
86. Tindell AJ, Berridge KC, Aldridge JW. 2004. Ventral pallidal representation of Pavlovian cues and reward: population and rate codes. J. Neurosci. 24:1058-69
87. Toates FM. 1986. Motivational Systems. Cambridge, UK: Cambridge Univ. Press. 188 pp.
88. Tully T, Quinn WG. 1985. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157:263-77
89. Unoki S, Matsumoto Y, Mizunami M. 2005. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur. J. Neurosci. 22:1409-16
90. Unoki S, Matsumoto Y, Mizunami M. 2006. Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur. J. Neurosci. 24:2031-38
91. Van Ree JM, Niesink RJ, Van Wolfswinkel L, Ramsey NF, Kornet MM, et al. 2000. Endogenous opioids and reward. Eur. J. Pharmacol. 405:89-101
92. Vergoz V, Roussel E, Sandoz JC, Giurfa M. 2007. Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS ONE 2:e288
93. Vlachou S, Markou A. 2010. GABAB receptors in reward processes. Adv. Pharmacol. 58:315-71
94. Waddell S. 2012. Roles for multiple amines in Drosophila appetitive memory. Nature. In press
95. White NM. 1989. Reward or reinforcement: What's the difference? Neurosci. Biobehav. Rev. 13:181-86
96. Wise RA. 1998. Drug-activation of brain reward pathways. Drug Alcohol Depend. 51:13-22
97. Wise RA. 2005. Forebrain substrates of reward and motivation. J. Comp. Neurol. 493:115-21
98. Wise RA, Bozarth MA. 1985. Brain mechanisms of drug reward and euphoria. Psychiatr. Med. 3:445-60
99. Wise RA, Rompre PP. 1989. Brain dopamine and reward. Annu. Rev. Psychol. 40:191-225
100. Wright GA, Mustard JA, Simcock NK, Ross-Taylor AAR, McNicholas LD, et al. 2010. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr. Biol. 20:2234-40
101. Wyvell CL, Berridge KC. 2000. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J. Neurosci. 20:8122-30
102. Zubieta JK, Smith YR, Bueller JA, Xu Y, Kilbourn MR, et al. 2001. Regionalμ-opioid receptor regulation of sensory and affective dimensions of pain. Science 293:311-15