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WIREs Cogn Sci
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Learning and cognition in insects

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Insects possess small brains but exhibit sophisticated behavioral performances. Recent works have reported the existence of unsuspected cognitive capabilities in various insect species, which go beyond the traditional studied framework of simple associative learning. In this study, I focus on capabilities such as attention, social learning, individual recognition, concept learning, and metacognition, and discuss their presence and mechanistic bases in insects. I analyze whether these behaviors can be explained on the basis of elemental associative learning or, on the contrary, require higher‐order explanations. In doing this, I highlight experimental challenges and suggest future directions for investigating the neurobiology of higher‐order learning in insects, with the goal of uncovering l architectures underlying cognitive processing. WIREs Cogn Sci 2015, 6:383–395. doi: 10.1002/wcs.1348 This article is categorized under: Psychology > Learning Neuroscience > Behavior Neuroscience > Cognition
(a) Pavlovian olfactory conditioning of the proboscis extension response (PER) in restrained honeybees. Left panel: an individual bee is immobilized in a metal tube so that only the antennae and mouth parts (the proboscis) are free to move. The bee is set in front of an odorant stimulation setup which is controlled by a computer and which sends a constant flow of clean air to the bee. The air flow can be rerouted through cartridges presenting chemicals used for olfactory stimulation (conditioned stimuli or CS). Sucrose solution (unconditioned stimulus or US) is delivered by a toothpick to the antennae and to the proboscis. Right panel: After conditioning, the odor CS, which initially did not evoke any response, triggers the PER. (b) Operant visual conditioning of a tethered fruit fly (courtesy of B. Brembs). Left panel: A Drosophila is flying stationary in a cylindrical arena. The fly's tendency to perform left or right turns (yaw torque) is measured continuously and fed into a computer, which controls arena rotation. On the screen four ‘landmarks’, two Ts and two inverted Ts, are displayed in order to provide a referential frame for flight direction choice. A heat beam focused on the fly's thorax is used as an aversive reinforcer. The reinforcer is switched on whenever the fly flies toward a prohibitive direction. The fly controls therefore reinforcer delivery by means of its flight direction. Right panel: Detail of a tethered fly in suspended flight within the flight simulator.
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Metacognitive‐like processes in honey bees. (a) Experimental schedule. During the training, a horizontal black bar was used as the reference to define the above/below relationship. Targets were the same on both sides but variable between the 30 training trials. Reward (2 M sucrose) or punishment (quinine) was placed in a translucent microcentrifuge tube in the center of the targets. Within a trial, stimulus pairs were identical except for vertical position relative to the reference bar and relative to the bottom of the chamber. Between trials, targets and positions of targets and reference bars were varied so that bees could only learn the above/below relation of targets to the references as predictors of reward. In the example shown, the above relationship was rewarded and the below relationship punished. The transfer tests were unrewarded and used a novel target not used during the training. In the difficulty tests, the easiness of the discrimination was varied by changing the distance between the target and the horizontal of the reference bar. For easy trials, the target was clearly above or below the reference bar and did not overlap with the reference bar. For difficult trials, targets partially overlapped with the reference bar. For impossible trials, the center of both targets was in line with that of the reference bar. (b) Performance of bees. Proportion of correct choices as a function of blocks of five training trials (training) and performance in nonrewarded transfer test (red bar). Performance on tests varying in difficulty is also shown (green bars). Bees performed better on easy (83.8 ± 2.5%) than on difficult (52.4 ± 2.5%) or impossible tests (44.5 ± 7%) tests. (Reprinted with permission from Ref . Copyright 2013 National Academy of Sciences).
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Sameness learning in honey bees. (a) Y‐maze used to train bees in a delayed matching‐to‐sample task. Bees entered into the maze to collect sugar solution on one of the back walls of the maze. A sample was shown at the entrance before bees accessed the arms of the maze. (b) Training protocol. A group of bees were trained during 60 trials with black‐and‐white, vertical and horizontal gratings (Pattern Group); another group was trained with colours, blue and yellow (Colour Group). After training, both groups were subjected to a transfer test with novel stimuli (patterns for bees trained with colours, colours for bees trained with patterns). (c) Performance of the Pattern and the Colour Group in the transfer tests. Both groups chose the novel stimulus corresponding to the sample although they had no experience with such test stimuli. (Reprinted with permission from Ref . Copyright 2001 Nature Publishing Group, Macmillan Publishers Limited).
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Social learning in bumblebees—an elemental account. Percentage of choices by observer bees of a feeder occupied by a demonstrator bee. The arena contained eight feeders, four blue, and four yellow. The demonstrator was placed on one feeder type, yellow or blue, and the observer released in the arena. Right bar: Choices of the feeder occupied by a demonstrator in the first trial, when both feeder types were unfamiliar to observers. Left Bar: Choices of the alternative feeder type in subsequent trials when it was occupied by a demonstrator. The dashed line corresponds to a random choice in a situation where eight feeders were available. Asterisks correspond to P < 0.01. (Reprinted with permission from Ref . Copyright 2005 Cell Press). (b) Possible associations established by bumblebees during social learning in a foraging context. During direct interactions with demonstrators, observers experience nectar reward (US; green arrow) and associate demonstrators (conditioned stimulus 1 or CS1) with the US (red arrow); if demonstrators come to choose a novel feeder (here with a different color), observers will also land on the novel occupied feeder and will associate the physical properties of the flowers that demonstrators now exploit (CS2) with the demonstrators themselves (CS1; red arrow). The process postulated corresponds to a case of second‐order conditioning. (c) Nature of associations established during the two phases of a second‐order conditioning process.
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