Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

Abstract

SUMMARYThe natural history of adult worker honey bees (Apis mellifera) provides an opportunity to study the molecular basis of learning in an ecological context. Foragers must learn to navigate between the hive and floral locations that may be up to miles away. Young pre-foragers prepare for this task by performing orientation flights near the hive, during which they begin to learn navigational cues such as the appearance of the hive, the position of landmarks, and the movement of the sun. Despite welldescribed spatial learning and navigation behavior, there is currently limited information on the neural basis of insect spatial learning. We found that Egr, an insect homolog of Egr-1, is rapidly and transiently upregulated in the mushroom bodies in response to orientation. This result is the first example of an Egr-1 homolog acting as a learning-related immediate-early gene in an insect and also demonstrates that honey bee orientation uses a molecular mechanism that is known to be involved in many other forms of learning. This transcriptional response occurred both in naïve bees and in foragers induced to re-orient. Further experiments suggest that visual environmental novelty, rather than exercise or memorization of specific visual cues, acts as the stimulus for Egr upregulation. Our results implicate the mushroom bodies in spatial learning and emphasize the deep conservation of Egr-related pathways in experience-dependent plasticity.

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

“…1, "TF activity"), and a post hoc analysis identified 10 differentially expressed TFs (Table S2). Three of these, Egr2, Foxg1 (forkhead box G1), and Pitx1 (paired-like homeodomain 1), have been implicated in autism spectrum disorders (27)(28)(29), and Egr genes are also known to be socially responsive in birds and honey bees (30,31). The same TF-related GO term was enriched in the homologous triplet analysis (Dataset S5 and Fig.…”

Role of the different eyes in the visual odometry in the wolf spider Lycosa tarantula (Araneae, Lycosidae)

“…Additionally, the region of the MBs that receives visual information -the collar -is selectively developed when bees (Durst et al, 1994) or ants (Kühn-Bühlmann and Wehner, 2006;Stieb et al, 2010) begin to forage. The expression of an activity-dependent gene has been used to identify the MBs as a region that is active during navigation (Lutz and Robinson, 2013); this gene showed upregulated expression exclusively in the MBs after a single orientation flight.…”

Transcriptomic analysis of instinctive and learned reward-related behaviors in honey bees

“…Another transcription factor, egr, showed a strong increase in drone MB expression at the initiation of a mating flight. egr is involved in neuroplasticity in vertebrates (Knapska and Kaczmarek, 2004) and is upregulated in the MB of workers following an orientation flight (Lutz and Robinson, 2013). During orientation flights, bees learn the location of their hive relative to prominent landmarks and the position of the sun.…”

“…Brains were dissected to obtain samples containing the MB and surrounding nuclei (Fig. S1), following an established protocol (Sen Sarma et al, 2009;Lutz and Robinson, 2013;McNeill et al, 2016). RNA was extracted using Picopure RNA isolation kits (Applied Biosystems) and poly-adenylated RNA was enriched using Oligo(dT)25 Dynabeads (Thermo Fisher Scientific).…”

“…The mushroom bodies (MB), a region in the dorsal protocerebrum of the brain involved in multi-modal sensory processing, learning and memory (Zars, 2000), was selected for the present study, as it is involved in both instinctive (Sen Sarma et al, 2009;Lutz and Robinson, 2013;McNeill et al, 2016) and learned behavior. In addition, the MB also has recently been shown to show strong transcriptional responses to various types of food rewards (McNeill et al, 2016).…”