Mushroom Body Output Neurons Encode Odor–Reward Associations

Abstract

Neural correlates of learning and memory formation have been reported at different stages of the olfactory pathway in both vertebrates and invertebrates. However, the contribution of different neurons to the formation of a memory trace is little understood. Mushroom bodies (MBs) in the insect brain are higher-order structures involved in integration of olfactory, visual, and mechanosensory information and in memory formation. Here we focus on the ensemble spiking activity of single MB output neurons (ENs) when honeybees learned to associate an odor with reward. A large group of ENs (ϳ50%) changed their odor response spectra by losing or gaining sensitivity for specific odors. This response switching was dominated by the rewarded stimulus (CSϩ), which evoked exclusively recruitment. The remaining ENs did not change their qualitative odor spectrum but modulated their tuning strength, again dominated by increased responses to the CSϩ. While the bees showed a conditioned response (proboscis extension) after a few acquisition trials, no short-term effects were observed in the neuronal activity. In both EN types, associative plastic changes occurred only during retention 3 h after conditioning. Thus, long-term but not short-term memory was reflected by increased EN activity to the CSϩ. During retention, the EN ensemble separated the CSϩ most differently from the CSϪ and control odors ϳ140 ms after stimulus onset. The learned behavioral response appeared ϳ330 ms later. It is concluded that after memory consolidation, the ensemble activity of the MB output neurons predicts the meaning of the stimulus (reward) and may provide the prerequisite for the expression of the learned behavior.

Simultaneous Long-term Recordings at Two Neuronal Processing Stages in Behaving Honeybees

“…The described electrodes are suitable for recording both single unit and population activity which is especially useful for latency measurements and other temporal response properties of different neurons and different neuropils within a single specimen (for details see 1,2,25 ). Additionally we have shown how to permanently implement the micro wire electrodes to allow stable long-term recordings in behaving honeybees that last for hours up to days.…”

“…Insert another silver wire into the muscle projection region below the lateral ocelli. NOTE: If necessary the learning behavior of the bee can be monitored with high temporal precision by recording the muscle M17, which is involved in the proboscis extension response (PER) of the bee 36 as described in 25 . 3.…”

“…ENs responsible for olfactory information processing mostly innervate the ventral aspect of the vertical lobe 22 . Recently, it has been shown that ENs recorded at this area encode the odor reward association 25 .…”

Learning pattern recognition and decision making in the insect brain

“…This dynamics results from the interplay of excitatory and inhibitory neurons [74,81,82]. There is some debate about the function of temporal coding in behavior, because individuals react faster solving discrimination task than the structure of the temporal code indicates [83,84,85]. However there is evidence that by blocking inhibition in the AL insects lack the ability to discriminate between similar odors [33,74].…”

“…Advantages and challenges. The MP model is adequate to answer limits in performance of pattern recognition devices for fast operation which is sufficient to account for the fast reliable code observed in the AL [129,83,84,85]. It is also very useful to establish the equivalence with classical pattern recognition devices like the support vector machines (SVMs) [130,131,132,133,134].…”