Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

SummaryThe 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 [1-5]. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on de-novo protein synthesis [6, 7], require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones [8-17]. Compared to modulation of existing connections, the reorganization of circuits affords the unique possibility of sampling for potential new partners [18-20]. Nonetheless, only few examples of rewiring associated with learning have been established thus far [14, 21-24]. 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) [25]. 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.

Morphology and physiology of olfactory neurons in the lateral protocerebrum of the silkmoth Bombyx mori

Insect olfaction is a suitable model to investigate sensory processing in the brain. Olfactory information is first processed in the antennal lobe and is then conveyed to two second-order centres—the mushroom body calyx and the lateral protocerebrum. Projection neurons processing sex pheromones and plant odours supply the delta area of the inferior lateral protocerebrum (∆ILPC) and lateral horn (LH), respectively. Here, we investigated the neurons arising from these regions in the brain of the silkmoth, Bombyx mori, using mass staining and intracellular recording with a sharp glass microelectrode. The output neurons from the ∆ILPC projected to the superior medial protocerebrum, whereas those from the LH projected to the superior lateral protocerebrum. The dendritic innervations of output neurons from the ∆ILPC formed a subdivision in the ∆ILPC. We discuss pathways for odour processing in higher order centres.

Convergence of monosynaptic and polysynaptic sensory paths onto common motor outputs in a Drosophila feeding connectome

We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of Drosophila larvae. Input neurons originate from enteric, pharyngeal and external sensory organs and converge onto seven distinct sensory synaptic compartments within the CNS. Output neurons consist of feeding motor, serotonergic modulatory and neuroendocrine neurons. Monosynaptic connections from a set of sensory synaptic compartments cover the motor, modulatory and neuroendocrine targets in overlapping domains. Polysynaptic routes are superimposed on top of monosynaptic connections, resulting in divergent sensory paths that converge on common outputs. A completely different set of sensory compartments is connected to the mushroom body calyx. The mushroom body output neurons are connected to interneurons that directly target the feeding output neurons. Our results illustrate a circuit architecture in which monosynaptic and multisynaptic connections from sensory inputs traverse onto output neurons via a series of converging paths.

The Feeding Connectome: Convergence of Monosynaptic and Polysynaptic Sensory Paths onto Common Motor Outputs

Little is known about the organization of central circuits by which external and internal sensory inputs act on motor outputs to regulate fundamental behaviors such as feeding. We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior ofDrosophilalarvae. The input neurons originate from enteric, pharyngeal and external sensory organs and converge onto seven distinct sensory synaptic compartments within the CNS, as defined by distribution patterns of their presynaptic sites. The output neurons consist of pharyngeal motor neurons, serotonergic modulatory neurons, and neuroendocrine neurons that target the ring gland, a key endocrine organ. Monosynaptic connections from a set of sensory synaptic compartments cover the motor and endocrine targets in overlapping domains. Polysynaptic routes can be superimposed on top of the monosynaptic connections, resulting in divergent sensory paths that converge on common motor outputs. A completely different set of sensory compartments is connected to the mushroom body calyx of the memory circuits. Our results illustrate a circuit architecture in which monosynaptic and multisynaptic connections from sensory inputs traverse onto output neurons via a series of converging paths.