Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee

PLoS Biol. 2023 Jan 31;21(1):e3001984. doi: 10.1371/journal.pbio.3001984. eCollection 2023 Jan.

Abstract

Understanding of the neural bases for complex behaviors in Hymenoptera insect species has been limited by a lack of tools that allow measuring neuronal activity simultaneously in different brain regions. Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the honey bee, and expressed the calcium indicator GCaMP6f under the control of the honey bee synapsin promoter. We show that GCaMP6f is widely expressed in the honey bee brain, allowing to record neural activity from multiple brain regions. To assess the power of this tool, we focused on the olfactory system, recording simultaneous responses from the antennal lobe, and from the more poorly investigated lateral horn (LH) and mushroom body (MB) calyces. Neural responses to 16 distinct odorants demonstrate that odorant quality (chemical structure) and quantity are faithfully encoded in the honey bee antennal lobe. In contrast, odor coding in the LH departs from this simple physico-chemical coding, supporting the role of this structure in coding the biological value of odorants. We further demonstrate robust neural responses to several bee pheromone odorants, key drivers of social behavior, in the LH. Combined, these brain recordings represent the first use of a neurogenetic tool for recording large-scale neural activity in a eusocial insect and will be of utility in assessing the neural underpinnings of olfactory and other sensory modalities and of social behaviors and cognitive abilities.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / genetics
  • Brain / physiology
  • Calcium*
  • Odorants
  • Pheromones / genetics
  • Smell* / genetics

Substances

  • Calcium
  • Pheromones

Associated data

  • Dryad/10.5061/dryad.83bk3j9tt

Grants and funding

We thank the French Research National Agency (ANR to JCS, Project ANR-17-CE20-0003 Bee-O-Choc; ANR to JC, Project ANR-22-CE37-0029 Pherobrain), the CNRS (JCS) and the University Paris-Saclay (JC and JCS), the DFG (Deutsche Forschungsgemeinschaft to MB) and CIMeC, University of Trento (AH) for funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.