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Multi-unit Recording Methods to Characterize Neural Activity in the Locust Schistocerca Americana Olfactory Circuits
Published on: January 25, 2013
Structured sampling of olfactory input by the fly mushroom body
Zhihao Zheng1, Feng Li2, Corey Fisher2
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544, USA; Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA; The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University, Baltimore, MD 21205, USA.
Abstract:
Associative memory formation and recall in the fruit fly Drosophila melanogaster is subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes a profound transformation from broadly tuned and stereotyped odorant responses in the olfactory projection neuron (PN) layer to narrowly tuned and nonstereotyped responses in the Kenyon cells (KCs). Theory and experiment suggest that this transformation is implemented by random connectivity between KCs and PNs. However, this hypothesis has been challenging to test, given the difficulty of mapping synaptic connections between large numbers of brain-spanning neurons. Here, we used a recent whole-brain electron microscopy volume of the adult fruit fly to map PN-to-KC connectivity at synaptic resolution. The PN-KC connectome revealed unexpected structure, with preponderantly food-responsive PN types converging at above-chance levels on downstream KCs. Axons of the overconvergent PN types tended to arborize near one another in the MB main calyx, making local KC dendrites more likely to receive input from those types. Overconvergent PN types preferentially co-arborize and connect with dendrites of αβ and α'β' KC subtypes. Computational simulation of the observed network showed degraded discrimination performance compared with a random network, except when all signal flowed through the overconvergent, primarily food-responsive PN types. Additional theory and experiment will be needed to fully characterize the impact of the observed non-random network structure on associative memory formation and recall.
Insights
Fruit fly mushroom bodies transform sensory input for memory. Researchers mapped neuron connections, finding non-random, food-odor focused pathways, challenging previous theories of random connectivity.
Area of Science:
- Neuroscience
- Computational Biology
- Animal Behavior
Background:
- Associative memory in Drosophila melanogaster relies on the mushroom body (MB).
- Sensory information transforms from broad olfactory projection neuron (PN) responses to narrow Kenyon cell (KC) responses within the MB.
- Previous hypotheses suggested random PN-KC connectivity underlies this transformation.
Purpose of the Study:
- To test the hypothesis of random PN-KC connectivity in the Drosophila MB.
- To map PN-to-KC synaptic connections at high resolution using whole-brain electron microscopy.
- To analyze the structural organization of PN-KC connectivity and its functional implications.
Main Methods:
- Utilized a whole-brain electron microscopy volume of adult fruit flies.
- Mapped synaptic connections between olfactory projection neurons (PNs) and Kenyon cells (KCs) at synaptic resolution.
- Performed computational simulations to assess network performance based on observed connectivity.
Main Results:
- The PN-KC connectome revealed a non-random structure, with food-responsive PN types converging non-randomly onto KCs.
- Overconvergent PN types showed preferential co-arborization and connectivity with specific KC subtypes (αβ and α'β').
- Computational models indicated degraded discrimination performance in the observed network compared to a random network, except under specific signal flow conditions.
Conclusions:
- The PN-KC network structure is not random, featuring specific convergence patterns related to odor response.
- This non-random connectivity may impact associative memory formation and recall.
- Further research is needed to fully elucidate the functional consequences of this observed network architecture.

