Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain

Abstract

Each fall, eastern North American monarch butterflies (Danaus plexippus) use a time-compensated sun compass to migrate to their overwintering grounds in central Mexico. The sun compass mechanism involves the neural integration of skylight cues with timing information from circadian clocks to maintain a constant heading. The neuronal substrates for the necessary interactions between compass neurons in the central complex, a prominent structure of the central brain, and circadian clocks are largely unknown. To begin to unravel these neural substrates, we performed 3D reconstructions of all neuropils of the monarch brain based on anti-synapsin labeling. Our work characterizes 21 well-defined neuropils (19 paired, 2 unpaired), as well as all synaptic regions between the more classically defined neuropils. We also studied the internal organization of all major neuropils on brain sections, using immunocytochemical stainings against synapsin, serotonin, and γ-aminobutyric acid. Special emphasis was placed on describing the neuroarchitecture of sun-compass-related brain regions and outlining their homologies to other migratory species. In addition to finding many general anatomical similarities to other insects, interspecies comparison also revealed several features that appear unique to the monarch brain. These distinctive features were especially apparent in the visual system and the mushroom body. Overall, we provide a comprehensive analysis of the brain anatomy of the monarch butterfly that will ultimately aid our understanding of the neuronal processes governing animal migration.

Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations

“…MeTu neurons providing input to the AVP form dendritic branches within the boundary region of distal and proximal medulla [21,22,43]. The target neuropil innervated by MeTu neurons is the lateral/intermediate part of the AOTU, called the “lower unit or lower unit complex” of the AOTU (AOTU-LU or LUC) in locust and other insects [1,39,44]. Two classes of neurons, TuLAL1a and TuLAL1b, likely counterparts of the TuBu neurons described in this paper, form two parallel pathways that convey the output from the AOTU-LUC to small neuropil foci within the LAL which are homologous to the bulb, formerly called the lateral triangle and median olive.…”

Discordant timing between antennae disrupts sun compass orientation in migratory monarch butterflies

“…Both outputs have been demonstrated in monarch butterflies 16 but whether either of these neural outputs contains the relevant timing information remains to be determined. No direct connection between the two antennal lobes exists to our knowledge.…”

Immunocytochemical Localization of Amines and GABA in the Optic Lobe of the Butterfly, Papilio xuthus

“…Based on histological criteria, eight medulla layers are also distinguished in the butterfly, Pieris brassicae [36], and ten layers in the monarch butterfly, Danaus plexippus [43].…”