Circuit reorganization in theDrosophilamushroom body calyx accompanies memory consolidation

Abstract

The capacity of utilizing past experience to guide future action is a fundamental and conserved function of the nervous system. Associative memory formation initiated by the coincident detection of a conditioned stimulus (CS, e.g. odour) and an unconditioned stimulus (US, e.g. sugar reward) can lead to a short-lived memory trace (STM) within distinct circuits. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on de-novo protein synthesis, require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones. Compared to modulation of existing connections, the reorganization of circuits affords the unique possibility of sampling for potential new partners. Nonetheless, only few examples of rewiring associated with learning have been established thus far. Here, we report that memory consolidation is associated with the structural and functional reorganization of an identified circuit in the adult fly brain. The formation and retrieval of olfactory associative memories in Drosophila requires the mushroom body (MB). We identified the individual synapses of olfactory projection neurons (PNs) that deliver a conditioned odour to the MB and reconstructed the complexity of the microcircuit they form. Combining behavioural experiments with high-resolution microscopy and functional imaging, we demonstrated that the consolidation of appetitive olfactory memories closely correlates with an increase in the number of synaptic complexes formed by the PNs that deliver the conditioned stimulus and their postsynaptic partners. These structural changes result in additional functional synaptic connections.

Neural correlates for neonicotinoid-induced impairment of olfactory long-term memory

“…The firing of Kenyon cells is highly odour specific and allows the discrimination of similar odours in fruit flies 43 . Olfactory long-term memory formation was shown to increase both the number of MG on the projection neurons processing the CS 12 and the number of Kenyon cells responding to the CS 44 . The elevated number of MG in the lip of treated bees in our study might have led to the activation of a larger number of Kenyon cells by the CS during the memory test, thereby reducing bees’ ability to identify it and to retrieve the learned CS-US association.…”

“…Yet, we used a different method to quantify MG density, sampling a larger subregion of the lip 25 . In Drosophila an increase in MG number was shown to be specific to the projection neurons activated by the CS 12 . Since odours were shown to specifically activate a sparse number of MG in honey bees 39 , likely, the structural changes occurring in a subset of projection neurons were not detectable when quantifying the overall MG density.…”

“…Variation in MG number with age and sensory experience has received growing attention in the past decade 9,10 . An increase in the number of MG has been reported in honey bees and fruit flies following paired presentations of an odour (CS) and a sucrose reward (US) 11,12 . In these studies, the blockade of long-term memory (LTM) formation by unpairing the CS and US stimuli or by using inhibitors of transcription/protein synthesis prevented such plasticity of projection neurons.…”

Learning-dependent structural plasticity of intracortical and sensory connections to functional domains of the olfactory tubercle

“…Learningdependent plasticity of the sensory connection from the OB to OT domains may represent strong adaptive linkage of odor information to behavioral outputs (Doty, 1986). In drosophila, appetitive odor learning reorganized structural connectivity from the antennal lobe, the homolog of mammalian OB, to the mushroom body, the homolog of the olfactory cortex, in an odor input-specific manner (Baltruschat et al, 2021). In zebrafish, appetitive odor learning induced remapping of odor representation in the posterior zone of the dorsal telencephalon, the homolog of olfactory cortex, while underlying plasticity in neuronal connectivity remains unknown (Frank et al, 2019).…”