Neural correlates of odor learning in the honeybee antennal lobe.

Extracellular spiking activity and local field potentials (LFP) were recorded via tetrodes at the output of the antennal lobe (AL) in the honeybee brain during olfactory conditioning. Odors induce reliable rate responses that consist of either phasic-tonic responses, or complex responses with odor-specific profiles. In addition, odors evoke consistent responses of LFP oscillations in the 50-Hz band during the phasic ON-response to odor stimulation, and variable LFP responses at other frequency bands during the sustained response. A principal component analysis of the ensemble activity during differential conditioning consistently indicates the largest changes in response to the learned odor (conditioned stimulus; CS+). Relative LFP power increases for CS+ in the 15-40-Hz frequency band during the sustained response, and decreases for frequencies above 45 Hz. To quantify the relationship between these population responses given by the ensemble spiking activity and LFP, we show that for CS+ the learning-related changes in the degree of the phase-locked spiking activity correlate with the power changes in the corresponding frequency bands. Our results indicate associative plasticity in the AL of the bee leading to both enhancement and decrease of neuronal response rates. LFP power changes and the correlated changes in the locking between spikes and LFP at different frequencies observed for the learned odor serve as further evidence for a learning-induced restructuring of temporal ensemble representations.