Review Article | Published:

The honeybee as a model for understanding the basis of cognition

Nature Reviews Neuroscience volume 13, pages 758768 (2012) | Download Citation

Abstract

Honeybees contradict the notion that insect behaviour tends to be relatively inflexible and stereotypical. Indeed, they live in colonies and exhibit complex social, navigational and communication behaviours, as well as a relatively rich cognitive repertoire. Because these relatively complex behaviours are controlled by a brain consisting of only 1 million or so neurons, honeybees offer an opportunity to study the relationship between behaviour and cognition in neural networks that are limited in size and complexity. Most recently, the honeybee has been used to model learning and memory formation, highlighting its utility for neuroscience research, in particular for understanding the basis of cognition.

Key points

  • Honeybees with their tiny brains exhibit complex social and navigational behaviours and possess a relatively rich cognitive repertoire. A unique feature of honeybee behaviour is the waggle dance, a ritualized movement that communicates locations and their properties.

  • The honeybee brain consists of 1 million neurons that are structured in highly ordered neuropils. Many of the central neurons are individually identifiable and some of them are registered in a three-dimensional virtual standard brain atlas.

  • Cognitive forms of learning in the bee include categorization, extraction of dependences on context, sequences and combinations, and evaluation of sequential reward values.

  • The search for neural correlates of learning and memory processing in the honeybee is facilitated by a highly versatile behavioural paradigm: the classical conditioning of the proboscis extension response. This paradigm allows the monitoring of neural events in defined neural networks and single neurons together with behavioural change.

  • Learning-related plasticity is found in all neural components of the olfactory pathway and in an identified reward neuron. The sparse and combinatorial code of odours is predominantly enhanced for the learned odour at the input site of the mushroom body, whereas the mushroom body output codes the value of the learned signals.

  • Memory as characterized by behavioural and molecular studies is processed in four distinct phases in honeybees, which is similar to common properties of memory in other animal species.

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References

  1. 1.

    Intelligence without representation. Artif. Intell. 47, 139–159 (1991).

  2. 2.

    Honey bees as a model for vision, perception, and cognition. Annu. Rev. Entomol. 55, 267–284 (2010). An excellent review on the visual system of the honeybee.

  3. 3.

    & Cognitive architecture of a mini-brain: the honeybee. Trends Cognitive Sci. 5, 62–71 (2001).

  4. 4.

    , & Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (Springer, 2011). This book is a highly valuable and recent review on the state of the art in honeybee behaviour and neurobiology.

  5. 5.

    The Dance Language and Orientation of Bees (The Belknap Press of Harvard Univ. Press,1967). A bible for all researchers working with honeybees. Von Frisch describes in lucid words his lifelong research and discoveries.

  6. 6.

    An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59–63 (1993). This study showed that one single neuron in the bee brain, the VUMmx1, represents the neural substrate of reward during olfactory learning.

  7. 7.

    , , & Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J. Neurosci. 27, 11736–11747 (2007). This is the first study to use long-lasting extracellular recordings from honeybee mushroom body extrinsic neurons during olfactory learning.

  8. 8.

    , & Mushroom body output neurons encode odor reward associations. J. Neurosci. 31, 3129–3140 (2011).

  9. 9.

    , , , & Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J. Neurophysiol. 94, 3303–3313 (2005).

  10. 10.

    Neural correlates of olfactory learning in an identified neuron in the honey bee brain. J. Neurophysiol. 69, 609–625 (1993).

  11. 11.

    et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21, 1–11 (2011).

  12. 12.

    , , , & The Drosophila standard brain. Curr. Biol. 12, 227–231 (2002).

  13. 13.

    et al. The Virtual Fly Brain browser and query interface. Bioinformatics 28, 411–415 (2012).

  14. 14.

    et al. A three-dimensional average-shape atlas of the honeybee brain and its applications. J. Comp. Neurol. 492, 1–19 (2005). The standard brain atlas of the honeybee is introduced in this paper.

  15. 15.

    et al. The digital bee brain: integrating and managing neurons in a common 3D reference system. Front Syst. Neurosci. 4, 30 (2010).

  16. 16.

    Traces of Drosophila memory. Neuron 70, 8–19 (2011). A highly informative and most recent review of the neural correlates of memory processing in the Drosophila brain.

  17. 17.

    , & Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J. Neurosci. 31, 11772–11785 (2011).

  18. 18.

    et al. Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nature Neurosci. 15, 592–599 (2012).

  19. 19.

    & Learning and memory in the honeybee. J. Neurosci. 15, 1617–1630 (1995).

  20. 20.

    Behavioral theories and the neurophysiology of reward. Annu. Rev. Psychol. 57, 87–115 (2006).

  21. 21.

    , & Cognition in Invertebrates in Evolution of Nervous Systems, Vol. II: Evolution of Nervous Systems in Invertebrates (ed. Kaas, J. H.) 403–422 (Academic Press, 2007).

  22. 22.

    , & Conceptualization of above and below relationships by an insect. Proc. Biol. Sci. 278, 898–905 (2011).

  23. 23.

    , , , & The concepts of 'sameness' and 'difference' in an insect. Nature 410, 930–933 (2001).

  24. 24.

    , & Symmetry perception in an insect. Nature 382, 458–461 (1996).

  25. 25.

    & Dimensions of cognition in an insect, the honeybee. Behav. Cognitive Neurosci. Rev. 5, 24–40 (2006). This study reports the neural substrates of learning in the bee brain and other aspects of honeybee cognition.

  26. 26.

    , & Can animals recall the past and plan for the future? Nature Rev. Neurosci. 4, 685–691 (2003).

  27. 27.

    Serial position learning in honeybees. PLoS ONE 4, e4694–e4701 (2009).

  28. 28.

    , & Maze learning by honeybees. Neurobiol. Learn. Mem. 66, 267–282 (1996).

  29. 29.

    & Evidence for counting in insects. Anim. Cogn. 11, 683–689 (2008).

  30. 30.

    Working Memory (Oxford Univ. Press, 1986).

  31. 31.

    & Selective attention, working memory, and animal intelligence. Neurosci. Biobehav. Rev. 34, 23–30 (2010).

  32. 32.

    & Evolution of the brain and intelligence. Trends Cogn. Sci. 9, 250–257 (2005).

  33. 33.

    , , , & Visual working memory in decision making by honey bees. Proc. Natl Acad. Sci. USA 102, 5250–5255 (2005).

  34. 34.

    & Memory dynamics and foraging strategies of honeybees. Behav. Ecol. Sociobiol. 32, 17–29 (1993).

  35. 35.

    , & Learning reward expectations in honeybees. Learn. Mem. 14, 491–496 (2007).

  36. 36.

    Memory dynamics in the honeybee. J. Comp. Physiol. A 185, 323–340 (1999).

  37. 37.

    & Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honey bees. Learn. Mem. 19, 54–66 (2012).

  38. 38.

    Learning in honeybees: from molecules to behaviour. Zoology 105, 313–320 (2002).

  39. 39.

    & Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J. Neurosci. 18, 4384–4392 (1998).

  40. 40.

    Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27, 159–168 (2000).

  41. 41.

    , & Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J. Neurosci. 24, 4460–4468 (2004).

  42. 42.

    , & Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5, 343–358 (1980).

  43. 43.

    et al. Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. J. Neurosci. 30, 7817–7825 (2010).

  44. 44.

    , & Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. J. Neurosci. 25, 11614–11618 (2005).

  45. 45.

    , , , & Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain? J. Neurosci. 30, 6461–6465 (2010).

  46. 46.

    & Cognitive neuroepigenetics: a role for epigenetic mechanisms in learning and memory. Neurobiol. Learn. Mem. 96, 2–12 (2011).

  47. 47.

    et al. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8, e1000506 (2010).

  48. 48.

    , & Involvement of DNA methylation in memory processing in the honey bee. Neuroreport 21, 812–816 (2010).

  49. 49.

    Bee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee, Apis mellifera. Nature 443, 931–949 (2006).

  50. 50.

    , & Reversible downregulation of PKA during olfatory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. J. Neurosci. 19, 10125–10134 (1999).

  51. 51.

    , , & Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neurosci. 23, 5370–5380 (2003).

  52. 52.

    et al. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454, 519–522 (2008).

  53. 53.

    Einige Hypothesen über den anatomischen Mechanismus der Ideenbildung, der Assoziation und der Aufmerksamkeit. Archiv. Anatomie Physiol. 25, 367–378 (1895) (in German).

  54. 54.

    Santiago Ramón y Cajal and the croonian lecture, March 1894. Trends Neurosci. 17, 190–192 (1994).

  55. 55.

    , , , & Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15, 1953–1960 (2005).

  56. 56.

    , & Associative and non-associative plasticity in Kenyon cells of the honeybee mushroom body. Front. Syst. Neurosci. 2, 1–10 (2008). This paper highlights the strength of Ca2+ imaging, and reports the first data on neural correlates of associative learning in the dendrites of mushroom body intrinsic neurons.

  57. 57.

    , & Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha lobe. J. Comp. Neurol. 334, 444–65 (1993).

  58. 58.

    & Sensory representation and learning-related plasticity in mushroom body extrinsic feedback neurons of the protocerebral tract. Front. Syst. Neurosci. 4, 1–16 (2010).

  59. 59.

    , , , & Comparison of associative learning-related signals in the macaque perirhinal cortex and hippocampus. Cereb. Cortex 19, 1064–1078 (2008).

  60. 60.

    , , & Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron 67, 25–32 (2010).

  61. 61.

    , & Integrating hippocampus and striatum in decision-making. Curr. Opin. Neurobiol. 17, 692–697 (2007).

  62. 62.

    , & Learning substrates in the primate prefrontal cortex and striatum: sustained activity related to successful actions. Neuron 63, 244–253 (2009).

  63. 63.

    , & Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex. Nature Rev. Neurosci. 10, 141–152 (2009).

  64. 64.

    Social context, stress, and plasticity of aging. Aging Cell 10, 18–27 (2011).

  65. 65.

    , , & Size-related variation in protein abundance in the brain and abdominal tissue of bumble bee workers. Insect Mol. Biol. 21, 319–325 (2012).

  66. 66.

    , & DNA methylation changes elicited by social stimuli in the brains of worker honey bees. Genes Brain Behav. 11, 235–242 (2012).

  67. 67.

    et al. Queen pheromone modulates brain dopamine function in worker honey bees. Proc. Natl Acad. Sci. USA 104, 2460–2464 (2007).

  68. 68.

    Schwarmbienen auf Wohnungssuche. Z. Vgl. Physiol. 37, 263–324 (1955) (in German).

  69. 69.

    & Sensory coding of nest-site value in honeybee swarms. J. Exp. Biol. 211, 3691–3697 (2008).

  70. 70.

    , & Independence and interdependence in collective decision making: an agent-based model of nest-site choice by honeybee swarms. Phil. Trans. R. Soc. B 364, 755–762 (2009).

  71. 71.

    , & Choosing the greater of two goods: neural currencies for valuation and decision making. Nature Rev. Neurosci. 6, 363–375 (2005).

  72. 72.

    et al. On optimal decision-making in brains and social insect colonies. J. R. Soc. Interface 6, 1065–1074 (2009).

  73. 73.

    et al. Stop signals provide cross inhibition in collective decision-making by honeybee swarms. Science 335, 108–111 (2012).

  74. 74.

    & Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav. Ecol. Sociobiol. 24, 317–323 (1989).

  75. 75.

    & The honeybee waggle dance: can we follow the steps? Trends Ecol. Evol. 24, 242–247 (2009).

  76. 76.

    et al. A common frame of reference for learned and communicated vectors in honeybee navigation. Curr. Biol. 21, 645–650 (2011).

  77. 77.

    et al. Honeybees navigate according to a map-like spatial memory. Proc. Natl Acad. Sci. USA 102, 3040–3045 (2005). Using a novel device to track bees in flight, this reports the first convincing data that honeybees navigate according to Tolman's definition of a cognitive map.

  78. 78.

    , , , & Vector integration and novel shortcutting in honeybee navigation. Apidologie 43, 229–243 (2012).

  79. 79.

    , & Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69–89 (2008).

  80. 80.

    & Spatial maps in frontal and prefrontal cortex. Neuroimage 29, 567–577 (2006).

  81. 81.

    Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 13, 458–464 (1957) (in German). This study was the first to document that restrained bees can be conditioned to a stimulus, in this case a visual stimulus.

  82. 82.

    Classical conditioned response in the honey bee. J. Insect Physiol. 6, 168–179 (1961).

  83. 83.

    , , & Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107–119 (1983). This paper reports the first in-depth psychological analysis of olfactory conditioning using the proboscis extension response paradigm.

  84. 84.

    , , & Behavioural pharmacology in classical conditioning of the proboscis extension response in honeybees (Apis mellifera). J. Vis. Exp. 24, 2282 (2011).

  85. 85.

    , , , & Ant navigation: one-way routes rather than maps. Curr. Biol. 16, 75–79 (2006).

  86. 86.

    & Local and global navigational coordinate systems in desert ants. J. Exp. Biol. 212, 901–905 (2009).

  87. 87.

    Cognitive maps in rats and men. Psychol. Rev. 55, 189–208 (1948).

  88. 88.

    & The Hippocampus as a Cognitive Map (Oxford Univ. Press, 1978).

  89. 89.

    et al. Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403, 537–540 (2000).

  90. 90.

    , , & Honeybee navigation: nature and calibration of the “odometer”. Science 287, 851–853 (2000).

  91. 91.

    , & Long- but not medium-term retention of olfactory memories in honeybees is impaired by Actinomycin D and Anisomycin. Eur. J. Neurosci. 10, 2742–2745 (1998).

  92. 92.

    The brain of the honeybee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Phil. Trans. R. Soc. Lond. B 298, 309–354 (1982).

  93. 93.

    in Invertebrate Neurobiology (eds North, G. & Greenspan, R. J.) 53–78 (Cold Spring Harbor, 2007).

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Acknowledgements

I am grateful to D. Eisenhardt, B. Brembs, J. Rybak and G. Leboulle for commenting on an earlier version of the manuscript. I am particularly grateful to G. Leboulle for advice on the molecular genetic studies in honeybees, and to J. Rybak for his comments about the anatomy of the insect brain. My work is supported by the Deutsche Forschungsgemeinschaft, Gemeinnützige Stiftung Hertie and Klaus Tschira Stiftung.

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Affiliations

  1. Institute of Biology - Neurobiology, Free University of Berlin, 28/30 Königin-Luise-Strass, D-14195 Berlin, Germany.  menzel@neurobiologie.fu.berlin.de

    • Randolf Menzel

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The author declares no competing financial interests.

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https://doi.org/10.1038/nrn3357

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