Insect cognition

Last updated
A neuron (green and white) in an insect brain (blue) Insect neuron.png
A neuron (green and white) in an insect brain (blue)

Insect cognition describes the mental capacities and study of those capacities in insects. The field developed from comparative psychology where early studies focused more on animal behavior. [1] Researchers have examined insect cognition in bees, fruit flies, and wasps. [2] [3]  

Contents

Research questions consist of experiments aimed to evaluate insects abilities such as perception, [4] emotions [1] [5] attention, [3] memory (wasp multiple nest), [1] spatial cognition, [1] [6] tools use, [3] problem solving, [3] and concepts. [3] [7] Unlike in animal behavior the concept of group cognition plays a big part in insect studies. [7] [8] [9] It is hypothesized some insect classes like ants and bees think with a group cognition to function within their societies; [8] [9] more recent studies show that individual cognition exists and plays a role in overall group cognitive task. [5]

Insect cognition experiments have been more prevalent in the past decade than prior. [3] It is logical for the understanding of cognitive capacities as adaptations to differing ecological niches under the Cognitive faculty by species when analyzing behaviors, this means viewing behaviors as adaptations to an individual's environment and not weighing them more advanced when compared to other different individuals. [10]

Insect foraging cognition

Insects foraging on a yellow flower Yellow insects on yellow marigold.jpg
Insects foraging on a yellow flower

Insects inhabit many diverse and complex environments within which they must find food. Cognition shapes how an insect comes to find its food. The particular cognitive abilities used by insects in finding food has been the focus of much scientific inquiry. [11] The social insects are often study subjects and much has been discovered about the intelligence of insects by investigating the abilities of bee species. [12] [3] Fruit flies are also common study subjects. [13]

Learning and memory

Learning biases

Through learning, insects can increase their foraging efficiency, decreasing the time spent searching for food which allows for more time and energy to invest in other fitness related activities, such as searching for mates. Depending on the ecology of the insect certain cues may be used to learn to quickly identify food sources. Over evolutionary time insects may develop evolved learning biases that reflect the food source they feed on. [14]

Biases in learning allow insects to quickly associate relevant features of the environment that are related to food. For example, bees have an unlearned preference for radiating and symmetric patterns — features of natural flowers bees forage on. [15] Bees that have no foraging experience tend to have an unlearned preference for the colours that an experienced forager would learn faster. These colours tend to be those of highly rewarding flowers in that particular environment. [16]

Time-place learning

In addition to more typical cues like color and odor, insects are able to use time as a foraging cue. [17] Time is a particularly important cue for pollinators. Pollinators forage on flowers which tend to vary predictably in time and space, depending on the flower species, pollinators can learn the timing of blooming of flower species to develop more efficient foraging routes. Bees learn at which times and in which areas sites are rewarding and change their preference for particular sites based on the time of day. [18]

These time-based preferences have been shown to be tied to a circadian clock in some insects. In the absence of external cues honeybees will still show a shift in preference for a reward depending on time strongly implicating an internal time-keeping mechanism, i.e. the circadian clock, in modulating the learned preference. [17]

Moreover, not only can bees remember when a particular site is rewarding but they can also remember at what times multiple different sites are profitable. [18] Certain butterfly species also show evidence for time-place learning due to their trap-line foraging behaviour. [19] This is when an animal consistently visits the same foraging sites in a sequential manner across multiple days and is thought to be suggestive of a time-place learning ability.

Innovation capacity

A bumblebee with experience in the string-pulling task pulls the string to reach an artificial blue flower filled with sugar solution [20]

Insects are also capable of behavioral innovations. Innovation is defined as the creation of a new or modified learned behavior not previously found in the population. [21] Innovative abilities can be experimentally studied in insects through the use of problem solving tasks. [22] When presented with a string-pulling task, many bumblebees cannot solve the task, but a few can innovate the solution. [20]

Those that initially could not solve the task can learn to solve it by observing an innovator bee solving the task. These learned behaviors can then spread culturally through bee populations. [20] More recent studies in insects have begun to look at what traits (e.g. exploratory tendency) predict the propensity for an individual insect to be an innovator. [23]

Social aspects of insect foraging

Social learning of foraging sites

Insects can learn about foraging sites through observation or interaction with other individuals, termed social learning. This has been demonstrated in bumblebees. Bumblebees become attracted to rewarding flowers more quickly if they are occupied by other bumblebees and more quickly learn to associate that flower species with reward. [24] Seeing a conspecific on a flower enhances preferences for flowers of that type. Additionally, bumblebees will rely more on social cues when a task is difficult compared to when a task is simple. [25]

Ants will show conspecifics food sites they have discovered in a process called tandem running. This is considered to be a rare instance of teaching, a specialized form of social learning, in the animal kingdom. [26] Teaching involves consistent interactions between a tutor and a pupil and the tutor typically incurs some sort of cost in order to transmit the relevant information to the pupil. In the case of tandem running the ant is temporarily decreasing its own foraging efficiency in order to demonstrate to the pupil the location of a foraging site.

Evidence for Cumulative culture

Studies in bumblebees have provided evidence that some insects show the beginnings of cumulative culture through the act of refining existing behaviours into more efficient forms. Bumblebees are able to improve upon a task where they must pull a ball to a particular location, a previously socially learned behaviour, by using a more optimal route compared to the route that their demonstrator used. [27] This demonstration of refinement of a previously observed existing behaviour could be considered a rudimentary form of cumulative culture, although this a highly controversial idea. It is important to say that true cumulative culture has been difficult to show in insects and indeed, in all species. This would require culture accumulating over generations to the point where no single individual could independently generate the entire behaviour. [28]

Neural basis of insect foraging

Role of mushroom bodies

A diagram of a fruit fly mushroom body D. melanogaster mushroom body.png
A diagram of a fruit fly mushroom body

One important and highly studied brain region involved in insect foraging are the mushroom bodies, a structure implicated in insect learning and memory abilities. The mushroom body consists of two large stalks called peduncles which have cup-shaped projections on their ends called calyces. The role of the mushroom bodies is in sensory integration and associative learning. [29] They allow the insect to pair sensory information and reward. [29]

Experiments where the function of the mushroom bodies are impaired through ablation find that organisms are behaviourally normal but have impaired learning. Flies with impaired mushroom bodies cannot form an odour association [30] and cockroaches with impaired mushroom bodies cannot make use of spatial information to form memories about locations. [31] Electrophysiological underpinnings of the cognition in different parts of the insect brain can be studied by various techniques including in vivo recordings from these parts of the insect brain.

Mushroom body plasticity

Mushroom bodies can change in size throughout the lifespan of an insect. There is evidence these changes are related to the onset of foraging as well as the experience of foraging. In some Hymenoptera mushroom bodies increase in size when nurses become foragers and begin to forage for the colony. [32]

Young bees begin as nurses tending to the feeding and sanitation of the hive's larvae. As a bee ages it undergoes a shift in tasks from nurse to forager, leaving the hive to collect pollen. This shift in job leads to changes in gene expression within the brain which are associated with an increase in mushroom body size. [32]

Some butterflies have also been shown to undergo an experience-dependent increase in mushroom body size. [33] The period of greatest increase in brain size typically is associated with a period of learning through experiences with foraging demonstrating the importance of this structure in insect foraging cognition.

Mushroom body evolution

Multiple insect taxa have independently evolved larger mushroom bodies. The spatial cognition demands of foraging has been implicated in cases where more sophisticated mushroom bodies have evolved. [34] Cockroaches and bees, which are in different orders, both forage over a large area and make use of spatial information to return to foraging sites and central places which likely explains their larger mushroom bodies. [35] Contrast this with a dipteran such as the fruit fly Drosophila melanogaster , which has relatively small mushroom bodies and less complex spatial learning demands.

Related Research Articles

<span class="mw-page-title-main">Bumblebee</span> Genus of insect

A bumblebee is any of over 250 species in the genus Bombus, part of Apidae, one of the bee families. This genus is the only extant group in the tribe Bombini, though a few extinct related genera are known from fossils. They are found primarily in higher altitudes or latitudes in the Northern Hemisphere, although they are also found in South America, where a few lowland tropical species have been identified. European bumblebees have also been introduced to New Zealand and Tasmania. Female bumblebees can sting repeatedly, but generally ignore humans and other animals.

<span class="mw-page-title-main">Bee learning and communication</span> Cognitive and sensory processes in bees

Bee learning and communication includes cognitive and sensory processes in all kinds of bees, that is the insects in the seven families making up the clade Anthophila. Some species have been studied more extensively than others, in particular Apis mellifera, or European honey bee. Color learning has also been studied in bumblebees.

<span class="mw-page-title-main">Animal cognition</span> Intelligence of non-human animals

Animal cognition encompasses the mental capacities of non-human animals including insect cognition. The study of animal conditioning and learning used in this field was developed from comparative psychology. It has also been strongly influenced by research in ethology, behavioral ecology, and evolutionary psychology; the alternative name cognitive ethology is sometimes used. Many behaviors associated with the term animal intelligence are also subsumed within animal cognition.

<span class="mw-page-title-main">Waggle dance</span> Honey bees particular figure-eight dance

Waggle dance is a term used in beekeeping and ethology for a particular figure-eight dance of the honey bee. By performing this dance, successful foragers can share information about the direction and distance to patches of flowers yielding nectar and pollen, to water sources, or to new nest-site locations with other members of the colony.

<i>Hibiscus trionum</i> Species of flowering plant

Hibiscus trionum, commonly called flower-of-an-hour, bladder hibiscus, bladder ketmia, bladder weed, puarangi and venice mallow, is an annual plant native to the Old World tropics and subtropics. It has spread throughout southern Europe both as a weed and cultivated as a garden plant. It has been introduced to the United States as an ornamental where it has become naturalized as a weed of cropland and vacant land, particularly on disturbed ground.

<i>Bombus terrestris</i> Species of bee

Bombus terrestris, the buff-tailed bumblebee or large earth bumblebee, is one of the most numerous bumblebee species in Europe. It is one of the main species used in greenhouse pollination, and so can be found in many countries and areas where it is not native, such as Tasmania. Moreover, it is a eusocial insect with an overlap of generations, a division of labour, and cooperative brood care. The queen is monandrous which means she mates with only one male. B. terrestris workers learn flower colours and forage efficiently.

<span class="mw-page-title-main">Charles Henry Turner (zoologist)</span> African American zoologist, educator, and comparative psychologist

Charles Henry Turner was an American zoologist, entomologist, educator, and comparative psychologist, known for his studies on the behavior of insects, particularly bees and ants. Born in Cincinnati, Ohio, Turner was the first African American to receive a graduate degree at the University of Cincinnati and most likely the first African American to earn a PhD from the University of Chicago. He spent most of his career as a high school teacher in Sumner High School in St. Louis. Turner was one of the first scientists to systematically examine the question of whether animals display complex cognition, studying arthropods such as spiders and bees. He also examined differences in behavior between individuals within a species, a precursor to the study of animal personality.

<span class="mw-page-title-main">Palynivore</span> Group of herbivorous animals

In zoology, a palynivore /pəˈlɪnəvɔːɹ/, meaning "pollen eater" is an herbivorous animal which selectively eats the nutrient-rich pollen produced by angiosperms and gymnosperms. Most true palynivores are insects or mites. The category in its strictest application includes most bees, and a few kinds of wasps, as pollen is often the only solid food consumed by all life stages in these insects. However, the category can be extended to include more diverse species. For example, palynivorous mites and thrips typically feed on the liquid content of the pollen grains without actually consuming the exine, or the solid portion of the grain. Additionally, the list is expanded greatly if one takes into consideration species where either the larval or adult stage feeds on pollen, but not both. There are other wasps which are in this category, as well as many beetles, flies, butterflies, and moths. One such example of a bee species that only consumes pollen in its larval stage is the Apis mellifera carnica. There is a vast array of insects that will feed opportunistically on pollen, as will various birds, orb-weaving spiders and other nectarivores.

<span class="mw-page-title-main">Mate choice</span> One of the primary mechanisms under which evolution can occur

Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.

Comparative cognition is the comparative study of the mechanisms and origins of cognition in various species, and is sometimes seen as more general than, or similar to, comparative psychology. From a biological point of view, work is being done on the brains of fruit flies that should yield techniques precise enough to allow an understanding of the workings of the human brain on a scale appreciative of individual groups of neurons rather than the more regional scale previously used. Similarly, gene activity in the human brain is better understood through examination of the brains of mice by the Seattle-based Allen Institute for Brain Science, yielding the freely available Allen Brain Atlas. This type of study is related to comparative cognition, but better classified as one of comparative genomics. Increasing emphasis in psychology and ethology on the biological aspects of perception and behavior is bridging the gap between genomics and behavioral analysis.

<span class="mw-page-title-main">Trap-lining</span> Feeding strategy amongst certain families of birds

In ethology and behavioral ecology, trap-lining or traplining is a feeding strategy in which an individual visits food sources on a regular, repeatable sequence, much as trappers check their lines of traps. Traplining is usually seen in species foraging for floral resources. This involves a specified route in which the individual traverses in the same order repeatedly to check specific plants for flowers that hold nectar, even over long distances. Trap-lining has been described in several taxa, including bees, butterflies, tamarins, bats, rats, and hummingbirds and tropical fruit-eating mammals such as opossums, capuchins and kinkajous. Traplining is used to term the method in which bumblebees and hummingbirds go about collecting nectar, and consequently, pollinating each plant they visit. The term "traplining" was originally coined by Daniel Janzen, although the concept was discussed by Charles Darwin and Nikolaas Tinbergen.

Task allocation and partitioning is the way that tasks are chosen, assigned, subdivided, and coordinated within a colony of social insects. Task allocation and partitioning gives rise to the division of labor often observed in social insect colonies, whereby individuals specialize on different tasks within the colony. Communication is closely related to the ability to allocate tasks among individuals within a group. This entry focuses exclusively on social insects. For information on human task allocation and partitioning, see division of labour, task analysis, and workflow.

<span class="mw-page-title-main">Flower constancy</span> Tendency to visit certain flower species

Flower constancy or pollinator constancy is the tendency of individual pollinators to exclusively visit certain flower species or morphs within a species, bypassing other available flower species that could potentially contain more nectar. This type of foraging behavior puts selective pressures on floral traits in a process called pollinator-mediated selection. Flower constancy is different from other types of insect specialization such as innate preferences for certain colors or flower types, or the tendency of pollinators to visit the most rewarding and abundant flowers.

<span class="mw-page-title-main">Frequency-dependent foraging by pollinators</span> Animal behavior

Frequency-dependent foraging is defined as the tendency of an individual to selectively forage on a certain species or morph based on its relative frequency within a population. Specifically for pollinators, this refers to the tendency to visit a particular floral morph or plant species based on its frequency within the local plant community, even if nectar rewards are equivalent amongst different morphs. Pollinators that forage in a frequency-dependent manner will exhibit flower constancy for a certain morph, but the preferred floral type will be dependent on its frequency. Additionally, frequency-dependent foraging differs from density-dependent foraging as the latter considers the absolute number of certain morphs per unit area as a factor influencing pollinator choice. Although density of a morph will be related to its frequency, common morphs are still preferred when overall plant densities are high.

<span class="mw-page-title-main">Bumblebee communication</span>

Bumblebees, like the honeybee collect nectar and pollen from flowers and store them for food. Many individuals must be recruited to forage for food to provide for the hive. Some bee species have highly developed ways of communicating with each other about the location and quality of food resources ranging from physical to chemical displays.

<i>Bombus impatiens</i> Species of insect

Bombus impatiens, the common eastern bumble bee, is the most commonly encountered bumblebee across much of eastern North America. They can be found in the Eastern temperate forest region of the eastern United States, southern Canada, and the eastern Great Plains. Because of their great adaptability, they can live in country, suburbs, and even urban cities. This adaptability makes them a great pollinator species, leading to an increase in their commercial use by the greenhouse industry. This increase consequently led to their farther spread outside their previous distribution range. They are considered one of the most important species of pollinator bees in North America.

Aurore Avarguès-Weber is a French cognitive neuroscientist and ethologist who is researching the behaviour of bees at the Centre de Recherche sur la Cognition Animale in Toulouse.

Lars Chittka, FLS, FRES, FRSB is a German zoologist, ethologist and ecologist distinguished for his work on the evolution of sensory systems and cognition, using insect-flower interactions as a model.

<span class="mw-page-title-main">Martin Giurfa</span> Argentinean-French neurobiologist and neuroethologist

Martin Giurfa is an Argentinean-French neurobiologist and neuroethologist, member of the German National Academy of Sciences Leopoldina, the Académie royale des sciences, des lettres et des beaux-arts de Belgique, and the Institut Universitaire de France (IUF). He is acknowledged for his work on the neural mechanisms of cognition in invertebrates, which he mostly explores using honeybees as models for understanding basic principles of learning and memory.

Susan Denise Healy FRSE professor of biology at the University of St. Andrews, specialist in cognitive evolution and behavioural studies of birds and understanding the neurological basis of this. She was elected as a Fellow of the Royal Society of Edinburgh in 2021.

References

  1. 1 2 3 4 Burkhardt RW (1987). "The Journal of Animal Behavior and the early history of animal behavior studies in America". Journal of Comparative Psychology. 101 (3): 223–230. doi:10.1037/0735-7036.101.3.223. ISSN   0735-7036.
  2. Giurfa M (2014). "Cognition with few neurons: higher-order learning in insects". Trends in Neurosciences. 36 (5): 1 285–294. doi:10.1016/j.tins.2012.12.011. PMID   23375772. S2CID   7908013.
  3. 1 2 3 4 5 6 7 Perry CJ, Barron AB, Chittka L (2017). "The frontiers of insect cognition". Current Opinion in Behavioral Sciences. 16: 111–118. doi:10.1016/j.cobeha.2017.05.011. ISSN   2352-1546. S2CID   53184195.
  4. Giurfa M, Menzel R (1997). "Insect visual perception: complex abilities of simple nervous systems". Current Opinion in Neurobiology. 7 (4): 505–513. doi:10.1016/S0959-4388(97)80030-X. PMID   9287201. S2CID   7483311.
  5. 1 2 Baracchi D, Lihoreau M, Giurfa M (August 2017). "Do Insects Have Emotions? Some Insights from Bumble Bees". Frontiers in Behavioral Neuroscience. 11: 157. doi: 10.3389/fnbeh.2017.00157 . PMC   5572325 . PMID   28878636.
  6. Blackawton PS, Airzee S, Allen A, Baker S, Berrow A, Blair C, et al. (April 2011). "Blackawton bees". Biology Letters. 7 (2): 168–72. doi:10.1098/rsbl.2010.1056. PMC   3061190 . PMID   21177694.
  7. 1 2 Passino KM, Seeley TD, Visscher PK (2007-09-19). "Swarm cognition in honey bees". Behavioral Ecology and Sociobiology. 62 (3): 401–414. doi:10.1007/s00265-007-0468-1. ISSN   0340-5443. S2CID   1386639.
  8. 1 2 Wilson RA (September 2001). "Group-Level Cognition". Philosophy of Science. 68 (S3): S262–S273. doi:10.1086/392914. ISSN   0031-8248. S2CID   144160534.
  9. 1 2 Feinerman O, Korman A (January 2017). "Individual versus collective cognition in social insects". The Journal of Experimental Biology. 220 (Pt 1): 73–82. arXiv: 1701.05080 . Bibcode:2017arXiv170105080F. doi:10.1242/jeb.143891. PMC   5226334 . PMID   28057830.
  10. Giurfa M (May 2013). "Cognition with few neurons: higher-order learning in insects". Trends in Neurosciences. 36 (5): 285–94. doi:10.1016/j.tins.2012.12.011. PMID   23375772. S2CID   7908013.
  11. Jones PL, Agrawal AA (January 2017). "Learning in Insect Pollinators and Herbivores". Annual Review of Entomology. 62 (1): 53–71. doi:10.1146/annurev-ento-031616-034903. PMID   27813668.
  12. "Bees Have Small Brains But Big Ideas". Scientific American. doi:10.1038/scientificamericanmind0514-10b.
  13. Maimon G. "Could Fruit Flies Reveal the Hidden Mechanisms of the Mind?". Scientific American Blog Network. Retrieved 2020-01-30.
  14. Lehrer M, Horridge GA, Zhang SW, Gadagkar R (1995-01-30). "Shape vision in bees: innate preference for flower-like patterns" (PDF). Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 347 (1320): 123–137. Bibcode:1995RSPTB.347..123L. doi:10.1098/rstb.1995.0017. hdl: 1885/117351 . ISSN   0962-8436.
  15. Lehrer M, Horridge GA, Zhang SW, Gadagkar R (1995-01-30). "Shape vision in bees: innate preference for flower-like patterns" (PDF). Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 347 (1320): 123–137. Bibcode:1995RSPTB.347..123L. doi:10.1098/rstb.1995.0017. hdl: 1885/117351 . ISSN   0962-8436.
  16. Giurfa M, Nunez J, Chittka L, Menzel R (September 1995). "Colour preferences of flower-naive honeybees". Journal of Comparative Physiology A. 177 (3). doi:10.1007/BF00192415. ISSN   0340-7594. S2CID   36437846.
  17. 1 2 Zhang S, Schwarz S, Pahl M, Zhu H, Tautz J (November 2006). "Honeybee memory: A honeybee knows what to do and when". The Journal of Experimental Biology. 209 (Pt 22): 4420–8. doi:10.1242/jeb.02522. PMID   17079712. S2CID   262120047.
  18. 1 2 Pahl M, Zhu H, Pix W, Tautz J, Zhang S (October 2007). "Circadian timed episodic-like memory - a bee knows what to do when, and also where". The Journal of Experimental Biology. 210 (Pt 20): 3559–67. doi: 10.1242/jeb.005488 . hdl: 1885/18210 . PMID   17921157.
  19. Gilbert, Lawrence E. Raven, Peter H. (1980). Coevolution of animals and plants : Symposium V, First International Congress of Systematic and Evolutionary Biology, Boulder, Colorado, August 1973. University of Texas. ISBN   0-292-71056-9. OCLC   6511746.{{cite book}}: CS1 maint: multiple names: authors list (link)
  20. 1 2 3 Alem S, Perry CJ, Zhu X, Loukola OJ, Ingraham T, Søvik E, Chittka L (October 2016). Louis M (ed.). "Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect". PLOS Biology. 14 (10): e1002564. doi: 10.1371/journal.pbio.1002564 . PMC   5049772 . PMID   27701411.
  21. Reader SM, Laland KN (2003-09-25). "Animal Innovation: An Introduction". Animal Innovation. Oxford University Press. pp. 3–36. doi:10.1093/acprof:oso/9780198526223.003.0001. ISBN   978-0-19-852622-3.
  22. Griffin AS, Guez D (November 2014). "Innovation and problem solving: a review of common mechanisms". Behavioural Processes. 109 Pt B: 121–34. doi:10.1016/j.beproc.2014.08.027. PMID   25245306. S2CID   28550381.
  23. Collado MÁ, Menzel R, Sol D, Bartomeus I (2019-12-23). "Innovation in solitary bees is driven by exploration, shyness and activity levels". doi: 10.1101/2019.12.23.884619 .{{cite journal}}: Cite journal requires |journal= (help)
  24. Leadbeater E, Chittka L (2007-08-06). "The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris)". Behavioral Ecology and Sociobiology. 61 (11): 1789–1796. doi:10.1007/s00265-007-0412-4. ISSN   0340-5443. S2CID   569654.
  25. Baracchi D, Vasas V, Jamshed Iqbal S, Alem S (2018-01-13). Papaj D (ed.). "Foraging bumblebees use social cues more when the task is difficult". Behavioral Ecology. 29 (1): 186–192. doi: 10.1093/beheco/arx143 . ISSN   1045-2249.
  26. Franks NR, Richardson T (January 2006). "Teaching in tandem-running ants". Nature. 439 (7073): 153. Bibcode:2006Natur.439..153F. doi: 10.1038/439153a . PMID   16407943.
  27. Loukola OJ, Perry CJ, Coscos L, Chittka L (February 2017). "Bumblebees show cognitive flexibility by improving on an observed complex behavior". Science. 355 (6327): 833–836. Bibcode:2017Sci...355..833L. doi:10.1126/science.aag2360. PMID   28232576. S2CID   206651162.
  28. Schofield DP, McGrew WC, Takahashi A, Hirata S (December 2017). "Cumulative culture in nonhumans: overlooked findings from Japanese monkeys?". Primates. 59 (1): 113–122. Bibcode:2017Sci...355..833L. doi: 10.1007/s10329-017-0642-7 . PMC   5843669 . PMID   29282581.
  29. 1 2 Heisenberg M (April 2003). "Mushroom body memoir: from maps to models". Nature Reviews. Neuroscience. 4 (4): 266–75. doi:10.1038/nrn1074. PMID   12671643. S2CID   5038386.
  30. de Belle JS, Heisenberg M (February 1994). "Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies". Science. 263 (5147): 692–5. Bibcode:1994Sci...263..692D. doi:10.1126/science.8303280. PMID   8303280.
  31. Mizunami M, Weibrecht JM, Strausfeld NJ (1998-12-28). "Mushroom bodies of the cockroach: Their participation in place memory". The Journal of Comparative Neurology. 402 (4): 520–537. doi:10.1002/(sici)1096-9861(19981228)402:4<520::aid-cne6>3.0.co;2-k. ISSN   0021-9967. PMID   9862324. S2CID   44384958.
  32. 1 2 Whitfield CW, Cziko AM, Robinson GE (October 2003). "Gene expression profiles in the brain predict behavior in individual honey bees". Science. 302 (5643): 296–9. Bibcode:2003Sci...302..296W. doi:10.1126/science.1086807. PMID   14551438. S2CID   30489284.
  33. Montgomery SH, Merrill RM, Ott SR (June 2016). "Brain composition in Heliconius butterflies, posteclosion growth and experience-dependent neuropil plasticity". The Journal of Comparative Neurology. 524 (9): 1747–69. doi:10.1002/cne.23993. hdl: 2381/36988 . PMID   26918905. S2CID   20938927.
  34. Farris SM, Schulmeister S (March 2011). "Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects". Proceedings. Biological Sciences. 278 (1707): 940–51. doi:10.1098/rspb.2010.2161. PMC   3049053 . PMID   21068044.
  35. Farris SM, Van Dyke JW (December 2015). "Evolution and function of the insect mushroom bodies: contributions from comparative and model systems studies". Current Opinion in Insect Science. 12: 19–25. doi:10.1016/j.cois.2015.08.006.

Further reading