Shared visual attention and memory systems in the Drosophila brain

van Swinderen, Bruno, McCartney, Amber, Kauffman, Sarah, Flores, Kris, Agrawal, Kunal, Wagner, Jenee and Paulk, Angelique (2009) Shared visual attention and memory systems in the Drosophila brain. PLoS One, 4 6 Article e5989: 1-13. doi:10.1371/journal.pone.0005989


Author van Swinderen, Bruno
McCartney, Amber
Kauffman, Sarah
Flores, Kris
Agrawal, Kunal
Wagner, Jenee
Paulk, Angelique
Title Shared visual attention and memory systems in the Drosophila brain
Journal name PLoS One   Check publisher's open access policy
ISSN 1932-6203
1932-6203
Publication date 2009-06-01
Year available 2009
Sub-type Article (original research)
DOI 10.1371/journal.pone.0005989
Open Access Status DOI
Volume 4
Issue 6 Article e5989
Start page 1
End page 13
Total pages 13
Editor Christopher Surridge
Place of publication United States
Publisher Public Library of Science
Language eng
Subject C1
380303 Computer Perception, Memory and Attention
380101 Sensory Processes, Perception and Performance
270603 Animal Physiology - Systems
730104 Nervous system and disorders
730211 Mental health
780108 Behavioural and cognitive sciences
06 Biological Sciences
0606 Physiology
Abstract Background: Selective attention and memory seem to be related in human experience. This appears to be the case as well in simple model organisms such as the fly Drosophila melanogaster. Mutations affecting olfactory and visual memory formation in Drosophila, such as in dunce and rutabaga, also affect short-term visual processes relevant to selective attention. In particular, increased optomotor responsiveness appears to be predictive of visual attention defects in these mutants. Methodology/Principal Findings: To further explore the possible overlap between memory and visual attention systems in the fly brain, we screened a panel of 36 olfactory long term memory (LTM) mutants for visual attention-like defects using an optomotor maze paradigm. Three of these mutants yielded high dunce-like optomotor responsiveness. We characterized these three strains by examining their visual distraction in the maze, their visual learning capabilities, and their brain activity responses to visual novelty. We found that one of these mutants, D0067, was almost completely identical to dunce for all measures, while another, D0264, was more like wild type. Exploiting the fact that the LTM mutants are also Gal4 enhancer traps, we explored the sufficiency for the cells subserved by these elements to rescue dunce attention defects and found overlap at the level of the mushroom bodies. Finally, we demonstrate that control of synaptic function in these Gal4 expressing cells specifically modulates a 20-30 Hz local field potential associated with attention-like effects in the fly brain. Conclusions/Significance: Our study uncovers genetic and neuroanatomical systems in the fly brain affecting both visual attention and odor memory phenotypes. A common component to these systems appears to be the mushroom bodies, brain structures which have been traditionally associated with odor learning but which we propose might be also involved in generating oscillatory brain activity required for attention-like processes in the fly brain.
Formatted abstract
Background: Selective attention and memory seem to be related in human experience. This appears to be the case as well in simple model organisms such as the fly Drosophila melanogaster. Mutations affecting olfactory and visual memory formation in Drosophila, such as in dunce and rutabaga, also affect short-term visual processes relevant to selective attention. In particular, increased optomotor responsiveness appears to be predictive of visual attention defects in these mutants.

Methodology/Principal Findings: To further explore the possible overlap between memory and visual attention systems in the fly brain, we screened a panel of 36 olfactory long term memory (LTM) mutants for visual attention-like defects using an optomotor maze paradigm. Three of these mutants yielded high dunce-like optomotor responsiveness. We characterized these three strains by examining their visual distraction in the maze, their visual learning capabilities, and their brain activity responses to visual novelty. We found that one of these mutants, D0067, was almost completely identical to dunce1 for all measures, while another, D0264, was more like wild type. Exploiting the fact that the LTM mutants are also Gal4 enhancer traps, we explored the sufficiency for the cells subserved by these elements to rescue dunce attention defects and found overlap at the level of the mushroom bodies. Finally, we demonstrate that control of synaptic function in these Gal4 expressing cells specifically modulates a 20–30 Hz local field potential associated with attention-like effects in the fly brain.

Conclusions/Significance: Our study uncovers genetic and neuroanatomical systems in the fly brain affecting both visual attention and odor memory phenotypes. A common component to these systems appears to be the mushroom bodies, brain structures which have been traditionally associated with odor learning but which we propose might be also involved in generating oscillatory brain activity required for attention-like processes in the fly brain.
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

 
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Created: Sat, 15 Aug 2009, 00:55:30 EST by Debra McMurtrie on behalf of Queensland Brain Institute