The standardized central complex of the monarch butterfly brain: a tool for unravelling the neural basis of migratory behavior.
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1
University of Massachusetts Medical School, Neurobiology, United States
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2
Lund University, Biology, Sweden
The central complex (CX), a midline-spanning group of neuropils consisting of the upper and lower division of the central body (CBU, CBL), the protocerebral bridge (PB) and the noduli, has been implicated in many functions. Based on intracellular recordings in locusts, crickets, and monarch butterflies (Danaus plexippus), neuronal responses to simulated skylight cues suggest that a set of cells of the CX comprises a neuronal network that functions as an internal sun compass of the insect brain.
To further investigate this network in the monarch, we performed detailed analyses of neurobiotin-injected, single-neuron morphologies within the proposed compass neuropils. These neuropils include the CX, the lateral accessory lobes, and the anterior optic tubercles (AOTu). To aid our analysis, we established a standardized, shape-averaged atlas of these neuropils, which can serve as a common frame of reference for neuron registration and additionally provides a set of reference volumes. To test the utility of the standard, we registered more than 55 neurons belonging to 35 cell types into this common frame of reference. This was combined with high-resolution confocal imaging to characterize the individual arborization patterns of these cells. By means of interspecies comparisons, especially to the well-studied desert locust, we found conserved routes of information flow into the different monarch CX-components, as well as highly conserved intrinsic neurons and output pathways to the lateral accessory lobes. Species-specific differences were apparent mostly in neurons that were exclusively associated with the CBU, while most components of the compass network (those prominently innervating the PB and CBL) appeared to be highly conserved. This degree of conservation in the proposed compass network was surprising considering the large evolutionary distance between these species, and suggests the existence of a highly conserved core network of CX-neurons that likely underlies sun compass navigation and maybe even more general CX-functions such as the integration of multiple sensory modalities and spatial learning.
A role of the CX in mediating migratory behavior was further suggested by volumetric analysis. To test the usefulness of the reference volumes provided by the standardized compass neuropils, we compared these to additionally reconstructed neuropils in migratory monarchs and non-migratory, summer monarchs. In addition to the substantial increases in overall neuropil size linked to the increased lifespan of migratory monarchs, these comparisons revealed a specific increase in relative size of the PB and a decrease in relative size of the AOTu. These changes only occurred in animals that had undergone a large fraction of their fall migration. Moreover, correlation analysis revealed that only experienced migrants and summer monarchs (as opposed to reference monarchs without any behavioral experience) possessed highly size-correlated CX-neuropils, indicating that experience-dependent processes orchestrate changes of neuropil volumes in functionally linked brain regions.
Overall, these studies show that the standardized compass neuropils provide a useful tool to examine the anatomical basis of migratory behavior on multiple levels.
Keywords:
central complex,
Comparative Neuroanatomy,
compass navigation,
Lepidoptera,
polarized light,
Vision
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster Presentation (see alternatives below as well)
Topic:
Orientation and Navigation
Citation:
Heinze
S,
Florman
J,
Asokaraj
S,
El Jundi
B and
Reppert
SM
(2012). The standardized central complex of the monarch butterfly brain: a tool for unravelling the neural basis of migratory behavior..
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00166
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Received:
27 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Stanley Heinze, University of Massachusetts Medical School, Neurobiology, Worcester, MA, 01605, United States, stanley.heinze@biol.lu.se