Integrative analysis of multiple pathways in the honeybee olfactory system
Final Report Abstract
Animals face highly complex and dynamic olfactory stimuli in their natural environments, which require fast and reliable olfactory processing. Parallel processing is a common principle of sensory systems supporting this task, for example as known from visual and auditory systems, but its functional role in olfaction remained unclear. The presence of parallel olfactory subsystems represents a striking commonality across animal species. Examples are the main olfactory system, vomeronasal system, septal organ and Grueneberg organ in mammals and different subsystems present in amphibians, fish and insects, suggesting that parallel systems have a highly adaptive value. We use the honeybee Apis mellifera to study an insect species where two distinct olfactory subsystems of about equal size have been found within the main olfactory system: the lateral (l- ALT) and the medial (m-ALT) pathways of antennal lobe output neurons. In addition, the honeybee offers a large body of knowledge and a wealth of paradigms to study olfactory anatomy, physiology and behaviour, including learning and memory with close to cognitive capacities. We elaborated important new anatomical features of this dual olfactory pathway regarding modulatory systems, sex-specific differences in the subsystem-specific sensory supply, and differences in the synaptic divergence and plasticity of the two subsystems. Most importantly, using optophysiological recordings and real-time dual tract multi-unit electrophysiology we found that both antennal lobe output tracts respond to a largely similar panel of odors, but extract different features of olfactory information, indicating true parallel processing. Furthermore, we found evidence for at least two mechanisms of synaptic plasticity in the l-ALT subsystem following associative odor learning. Temporal analyses of coincident spiking activity of projection neurons within and across the m- and l-ALT revealed evidence for a temporal code suggesting that parallel processing and coincidence coding are combined processing strategies. In-situ patch clamp recordings revealed substantial differences of intrinsic electrical properties between projections neurons and Kenyon cells - suggesting that these intrinsic properties are important for olfactory coding. Triggered by these findings and the behavioural role of the fast temporal structure of natural odourant stimuli, we performed imaging analyses at the level of Kenyon cells in the mushroom bodies, partly by switching to Drosophila using genetically encoded calcium sensors, to further investigate processing temporal information at the Kenyon cell layer. Current analyses focus on intensity and mixture coding as well as the role of various forms of plasticity within the dual olfactory pathway and following odour pre-exposure, learning, and memory. The joint research programme of this tandem over the two funding periods of the SPP significantly advanced our understanding of parallel olfactory processing and temporal coding in this model system supporting the general significance of parallel olfactory subsystems in general.
Publications
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(2010) Parallel olfactory systems in insects: anatomy and function. Annual Rev Entomol 55: 399-420
Galizia CG, Rössler W
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(2012) Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera. J Comp Neurol 520:3509-3527
Groh C, Lu Z, Meinertzhagen IA, Rössler W
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(2012) The speed of smell: Odor-object segregation within milliseconds. PLoS ONE, 7: e36096
Szyszka P, Stierle JS, Biergans S, Galizia CG
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(2013) Millisecond stimulus onset-asynchrony enhances information about components in an odor mixture. J Neurosci 33:6060-6069
Stierle JS, Galizia CG, Szyszka P
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(2013) Parallel processing in the honeybee olfactory pathway: structure, function and evolution. J Comp Physiol A 199:981-996
Rössler W, Brill M
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(2013) Parallel processing via a dual olfactory pathway in the honeybee. J Neurosci 33(6):2443-2456
Brill MF, Rosenbaum T, Reus I, Kleineidam CJ, Nawrot MP, Rössler W
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(2014) Olfactory subsystems in the honeybee: sensory supply and sex-specificity. Cell Tissue Research 357:583-595
Kropf J, Kelber C, Bieringer K, Rössler W
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(2015) It takes two - coincidence coding within the dual olfactory pathway of the honeybee. Front Physiol 6:208
Brill MF, Meyer A, Rössler W
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(2017) A high-bandwidth dual-channel olfactory stimulator for studying temporal sensitivity of olfactory processing. Chemical Senses:42:141-151
Raiser G, Galizia CG, Szyszka P
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(2017) Trace conditioning in Drosophila induces associative plasticity in mushroom body Kenyon Cells and dopaminergic neurons. Frontiers in Neural Circuits 11-42. - eISSN 1662-5110
Dylla KV, Raiser G, Galizia CG, Szyszka P
