Abstract
To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells (KCs) of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral (APL) neuron in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic KCs. Combining electron microscopy (EM) data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the KCs requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.
Highlights
Every day we are challenged to navigate through a complex and variable environment, often characterized by similar stimuli combined in different ways
We found anterior paired lateral neuron (APL) to be highly involved in the MG structure, with pre- and post- synaptic contacts with both Kenyon cells (KCs) dendrites and projection neurons (PNs) boutons (Figure 1–figure supplement 1A) (Baltruschat et al 2021)
We found a 160 positive correlation between the number of synapses made by APL towards a specific PN and the reciprocal synapses formed by that PN onto APL (Figure 162 1D)
Summary
Every day we are challenged to navigate through a complex and variable environment, often characterized by similar stimuli combined in different ways. The ability to discriminate across stimuli is achieved by minimizing the overlap between patterns of neuronal activity through a process defined as “pattern separation” (Santoro 2013) This conserved property is intrinsic to diverse circuits such as the mammalian cerebellum, the dentate gyrus and the Drosophila mushroom body (MB) (Cayco-Gajic and Silver 2019). While PN odour-evoked activity is broadly tuned (Perez-Orive et al 2002; Bhandawat et al 2007), odour representation is sparse and decorrelated at the KCs layer (Honegger, Campbell, and Turner 2011; Turner, Bazhenov, and Laurent 2008; Campbell et al 2013b; Perez-Orive et al 2002), reducing overlap between stimuli representation and allowing for better discriminability (Kanerva 1988; Cayco-Gajic, Clopath, and Silver 2017; Olshausen and Field 2004). We suggest that the normalization of postsynaptic MG responses by APL is essential to determine the key property of KCs to respond only to the coincident input of PNs to multiple claws, allowing for an elevated stimulus discriminability
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