Visualization of a Distributed Synaptic Memory Code in the Drosophila Brain

During associative conditioning, animals learn which sensory cues are predictive for positive or negative conditions. Because sensory cues are encoded by distributed neurons, one has to monitor plasticity across many synapses to capture how learned information is encoded. We analyzed synaptic bouton...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2020-06, Vol.106 (6), p.963-976.e4
Main Authors: Bilz, Florian, Geurten, Bart R.H., Hancock, Clare E., Widmann, Annekathrin, Fiala, André
Format: Article
Language:English
Subjects:
Associative learning
Axonal plasticity
Axons
Behavior
Brain
Calcium signalling
Drosophila
Drosophila melanogaster
Information theory
insect brain
Insects
Kenyon cell
learning and memory
Mammals
Memory
Microscopy
Mineral oils
mushroom body
neuronal assemblies
Neurons
Odor
odor representation
olfactory coding
Olfactory discrimination learning
optical calcium imaging
Presynapse
Sensory evaluation
Synaptic plasticity
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Summary:During associative conditioning, animals learn which sensory cues are predictive for positive or negative conditions. Because sensory cues are encoded by distributed neurons, one has to monitor plasticity across many synapses to capture how learned information is encoded. We analyzed synaptic boutons of Kenyon cells of the Drosophila mushroom body γ lobe, a brain structure that mediates olfactory learning. A fluorescent Ca2+ sensor was expressed in single Kenyon cells so that axonal boutons could be assigned to distinct cells and Ca2+ could be measured across many animals. Learning induced directed synaptic plasticity in specific compartments along the axons. Moreover, we show that odor-evoked Ca2+ dynamics across boutons decorrelate as a result of associative learning. Information theory indicates that learning renders the stimulus representation more distinct compared with naive stimuli. These data reveal that synaptic boutons rather than cells act as individually modifiable units, and coherence among them is a memory-encoding parameter. [Display omitted] •Calcium activity is monitored in synaptic boutons of single Kenyon cells•Kenyon cell boutons are individually modifiable and act as functional units•Associative learning causes decorrelation of activity across synaptic boutons•Learning induces a gain in information rate coding across synaptic boutons Bilz et al. have used fruit flies to analyze how associative memories are encoded across distributed synapses within a brain. Using calcium imaging, they find that learning increases information throughput by changing coherent activity across synaptic boutons.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2020.03.010