Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies.

Previous electrophysiological studies of cockroach mushroom bodies demonstrated the sensitivity of efferent neurons to multimodal stimuli. The present account describes the morphology and physiology of several types of efferent neurons with dendrites in the medial lobes. In general, efferent neurons respond to a variety of modalities in a context-specific manner, responding to specific combinations or specific sequences of multimodal stimuli. Efferent neurons that show endogenous activity have dendritic specializations that extend to laminae of Kenyon cell axons equipped with many synaptic vesicles, termed "dark" laminae. Efferent neurons that are active only during stimulation have dendritic specializations that branch mainly among Kenyon cell axons having few vesicles and forming the "pale" laminae. A new category of "recurrent" efferent neuron has been identified that provides feedback or feedforward connections between different parts of the mushroom body. Some of these neurons are immunopositive to antibodies raised against the inhibitory transmitter gamma-aminobutyric acid. Feedback pathways to the calyces arise from satellite neuropils adjacent to the medial lobes, which receive axon collaterals of efferent neurons. Efferent neurons are uniquely identifiable. Each morphological type occurs at the same location in the mushroom bodies of different individuals. Medial lobe efferent neurons terminate in the lateral protocerebrum among the endings of antennal lobe projection neurons. It is suggested that information about the sensory context of olfactory (or other) stimuli is relayed by efferent neurons to the lateral protocerebrum where it is integrated with information about odors relayed by antennal lobe projection neurons.