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2015 ; 112
(43
): E5854-62
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Neural substrate for higher-order learning in an insect: Mushroom bodies are
necessary for configural discriminations
#MMPMID26460021
Devaud JM
; Papouin T
; Carcaud J
; Sandoz JC
; Grünewald B
; Giurfa M
Proc Natl Acad Sci U S A
2015[Oct]; 112
(43
): E5854-62
PMID26460021
show ga
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.