The connectome of the adultDrosophilamushroom body: implications for function

Abstract

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…As described in a companion paper on the MB (Li et al, 2020), about half of the mushroom body output neurons (MBONs) directly synapse onto FB tangential neurons that target the middle layers (4-6) of the FB ( Figure 46A). Some MBONs contact only a single type of FB tangential neuron, for example, MBON09 connects exclusively to FB4R (Figure 46Bi), but many other MBONs contact multiple downstream targets in the FB, for example, MBON04, which targets FB tangential neurons in both Layers 1 and 6 ( Figure 46Bii).…”

“…Prominent among these are a population of dorsal FB tangential neurons whose intrinsic excitability tracks sleep need and whose activation induces sleep (Donlea et al, 2011;Pimentel et al, 2016). FB tangential neurons also receive contextual input from the mushroom body (Dag et al, 2019;Li et al, 2020;Scaplen et al, 2020), an important center for learning and memory (reviewed in (Modi et al, 2020)). Together, the above evidence suggests that context-and state-dependent action selection, including initiating periods of behavioral quiescence, may be governed by the FB.…”

“…The MB is thought to be a center for associative learning (Cognigni et al, 2018;Modi et al, 2020). It receives inputs from nearly all sensory modalities and is innervated by multiple types of DANs (Li et al, 2020), and provides an architecture to flexibly convert sensory information from thousands of Kenyon cells (KCs) into experience-dependent (and DAN-mediated) valence signals carried by the MB's output neurons, the MBONs. MBONs broadcast these valence signals to other areas of the brain, but how these signals drive the fly's behavioral responses is not fully understood.…”

“…Some MBONs contact only a single type of FB tangential neuron, for example, MBON09 connects exclusively to FB4R (Figure 46Bi), but many other MBONs contact multiple downstream targets in the FB, for example, MBON04, which targets FB tangential neurons in both Layers 1 and 6 ( Figure 46Bii). MBONs of different neurotransmitter types, both excitatory and inhibitory, often converge onto the same FB tangential neurons (lines of different colors in Figure 28A; see (Li et al, 2020) for how neurotransmitters for each of the MBONs were identified). For example, the glutamatergic (and likely inhibitory) MBON04 and the cholinergic (excitatory) MBON12 both contact FB4A ( Figure 46A,Biii), and two MBONs that express different (likely) inhibitory neurotransmitters, MBON05 (glutamate) and MBON09 (GABA), converge onto FB4R, along with a third excitatory (cholinergic) MBON21 ( Figure 46A).…”

“…In some cases, we could use what is known about the KC inputs to different MBON types see (Li et al, 2020) to determine the type of sensory information in specific downstream FB tangential neurons (Figure 47 C,D). For example, several MBONs conveying valence signals associated with visual information send divergent streams of information to an intermediate layer of neurons in diverse brain regions.…”