Neuronal correlates of sleep in honey bees.

Journal: Neural networks : the official journal of the International Neural Network Society
Published Date:

Abstract

Honey bees Apis mellifera follow the day-night cycle for their foraging activity, entering rest periods during darkness. Despite considerable research on sleep behaviour in bees, its underlying neurophysiological mechanisms are not well understood, partly due to the lack of brain imaging data that allow for analysis from a network- or system-level perspective. This study aims to fill this gap by investigating whether neuronal activity during rest periods exhibits stereotypic patterns comparable to sleep signatures observed in vertebrates. Using two-photon calcium imaging of the antennal lobes (AL) in head-fixed bees, we analysed brain dynamics across motion and rest epochs during the nocturnal period. The recorded activity was computationally characterised, and machine learning was applied to determine whether a classifier could distinguish the two states after motion correction. Out-of-sample classification accuracy reached 93 %, and a feature importance analysis suggested network features to be decisive. Accordingly, the glomerular connectivity was found to be significantly increased in the rest-state patterns. A full simulation of the AL using a leaky spiking neural network revealed that such a transition in network connectivity could be achieved by weakly correlated input noise and a reduction of synaptic conductance of the inhibitive local neurons (LNs) which couple the AL network nodes. The difference in the AL response maps between awake- and sleep-like states generated by the simulation showed a decreased specificity of the odour code in the sleep state, suggesting reduced information processing during sleep. Since LNs in the bee brain are GABAergic, this suggests that the GABAergic system plays a central role in sleep regulation in bees as in many higher species including humans. Our findings support the theoretical view that sleep-related network modulation mechanisms are conserved throughout evolution, highlighting the bee's potential as an invertebrate model for studying sleep at the level of single neurons.

Authors

  • Sebastian Moguilner
    Global Brain Health Institute (GBHI), University of California San Francisco (UCSF), San Francisco, CA, USA; Global Brain Health Institute (GBHI), Trinity College Dublin, Dublin, Ireland; Latin American Brain Health (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile; Cognitive Neuroscience Center (CNC), Universidad de San Andrés, Buenos Aires, Argentina; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
  • Ettore Tiraboschi
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy.
  • Giacomo Fantoni
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy.
  • Heather Strelevitz
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy.
  • Hamid Soleimani
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy.
  • Luca Del Torre
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy.
  • Uri Hasson
    Princeton University, United States.
  • Albrecht Haase
    Center for Mind/Brain Sciences (CIMeC), University of Trento, Italy; Department of Physics, University of Trento, Italy. Electronic address: albrecht.haase@unitn.it.