Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees

Komischke, Bernhard; Sandoz, Jean‐Christophe; Lachnit, Harald; Giurfa, Martín

doi:10.1016/s0166-4328(03)00105-0

Cited by 36 publications

(42 citation statements)

References 43 publications

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“…Different variants of this Pavlovian protocol have been conceived to study nonelemental olfactory learning in honey bees. In particular, bees effectively learn negative patterning discriminations (A+, B+ vs. AB−; see the Introduction) and their reversed counterpart, positive patterning (A−, B− vs. AB+) (equivalent to the XOR and AND problems, respectively) (32)(33)(34)46). To determine whether MBs are required for both patterning discriminations, we combined these two conditioning problems with local procaine anesthesia to block neural activity specifically in these brain centers in a transient and reversible way (37,38).…”

Section: Resultsmentioning

confidence: 99%

“…They require the ability to establish configural associations: i.e., unique conjunctive representations of compound stimuli that can then be treated as different from the simple sum of their elements. Honey bees, like mammals, learn patterning discriminations using nonelemental strategies (32)(33)(34)46), a capacity that seems absent in other insect models of learning and memory (31,59). Prior work on patterning discriminations in bees focused on negative rather than on positive patterning (32-34) because elemental accounts exist for the latter but not for the former (32).…”

Section: Discussionmentioning

confidence: 99%

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Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

Devaud

Papouin

Carcaud

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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120

116

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Learning theories distinguish elemental from configural learning based on their different complexity. Although the former relies on simple and unambiguous links between the learned events, the latter deals with ambiguous discriminations in which conjunctive representations of events are learned as being different from their elements. In mammals, configural learning is mediated by brain areas that are either dispensable or partially involved in elemental learning. We studied whether the insect brain follows the same principles and addressed this question in the honey bee, the only insect in which configural learning has been demonstrated. We used a combination of conditioning protocols, disruption of neural activity, and optophysiological recording of olfactory circuits in the bee brain to determine whether mushroom bodies (MBs), brain structures that are essential for memory storage and retrieval, are equally necessary for configural and elemental olfactory learning. We show that bees with anesthetized MBs distinguish odors and learn elemental olfactory discriminations but not configural ones, such as positive and negative patterning. Inhibition of GABAergic signaling in the MB calyces, but not in the lobes, impairs patterning discrimination, thus suggesting a requirement of GABAergic feedback neurons from the lobes to the calyces for nonelemental learning. These results uncover a previously unidentified role for MBs besides memory storage and retrieval: namely, their implication in the acquisition of ambiguous discrimination problems. Thus, in insects as in mammals, specific brain regions are recruited when the ambiguity of learning tasks increases, a fact that reveals similarities in the neural processes underlying the elucidation of ambiguous tasks across species.learning | configural learning | mushroom bodies | honey bee | Apis mellifera

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

Devaud

Papouin

Carcaud

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

120

116

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“…The maintenance of MB architecture, as we demonstrated, may allow workers to remain adept at task performance. Hydroxyurea lesioning of the MB in honeybees and fruit flies results in diminished olfactory discrimination and impairment of associative learning, respectively [de Belle and Heisenberg, 1994;Komischke et al, 2003]. Similar chemical manipulations of brain development in P. dentata would be insightful.…”

Section: Neural and Behavioral Robustness And Brain Modularitymentioning

confidence: 99%

Behavioral Performance and Neural Systems Are Robust to Sensory Injury in Workers of the Ant Pheidole dentata

2017

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Miniaturized nervous systems have been thought to limit behavioral ability, and animals with miniaturized brains may be less flexible when challenged by injuries resulting in sensory deficits that impact the development, maintenance, and plasticity of small-scale neural networks. We experimentally examined how injuries to sensory structures critical for olfactory ability affect behavioral performance in workers of the ant Pheidole dentata, which have minute brains (0.01 mm³) and primarily rely on the perception and processing of chemical signals and cues to direct their social behavior. We employed unilateral antennal denervation to decrease the olfactory perception ability of workers and quantified consequential neuroanatomical and behavioral performance effects. Postablation neuroanatomical metrics revealed a 25% reduction in the volume of the antennal lobe ipsilateral to the antennal lesion relative to the contralateral lobe, indicating atrophy of the input-deprived tissue. However, antennectomy did not affect the volumes of the mushroom body or its subcompartments or the number of mushroom body synaptic complexes (microglomeruli) in either brain hemisphere. Synapsin immunoreactivity, however, was significantly higher in the ipsilateral mushroom body calyces, which could reflect presynaptic potentiation and homeostatic compensation in higher-order olfactory regions. Despite tissue loss caused by antennal lesioning and resulting unilateral sensory deprivation, the ability of workers to perform behaviors that encompass the breadth of their task repertoire and meet demands for colony labor remained largely intact. The few behavioral deficits recorded were restricted to pheromone trail-following ability, a result that was expected due to the need for bilateral olfactory input to process spatial odor information. Our macroscopic and cellular neuroanatomical measurements and assessments of task performance demonstrate that the miniaturized brains of P. dentata workers and their sensorimotor functions are remarkably robust to injury-related size reduction and remain capable of generating behaviors required to respond appropriately to chemical social signals and effectively nurse immatures, as well as participate in coordinated foraging.

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“…In the case of honeybee olfactory learning, computer simulations and experiments such as negative patterning and its variants (Deisig et al, 2001(Deisig et al, , 2002(Deisig et al, , 2003 showed that olfactory compound learning and processing in bees was consistent with the uniquecue theory. A unique cue is generated when bees receive olfactory input to both brain sides, since bilateral olfactory input is required to solve a negative patterning task (Komischke et al, 2003). Assuming that the elements interfered with each other is implied in a modified unique-cue theory (Redhead and Pearce, 1995), which provided the best account for all the behavioral results available (Deisig et al, 2003;Lachnit et al, 2004).…”

Section: Nonelemental Forms Of Associative Learningmentioning

confidence: 99%

Cognition in Invertebrates

Menzel

Brembs

Giurfa

2007

Evolution of Nervous Systems

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Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees

Cited by 36 publications

References 43 publications

Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

Behavioral Performance and Neural Systems Are Robust to Sensory Injury in Workers of the Ant Pheidole dentata

Cognition in Invertebrates

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