Valence and state-dependent population coding in dopaminergic neurons in the fly mushroom body

Abstract

<jats:title>Summary</jats:title><jats:p>Neuromodulation permits flexibility of synapses, neural circuits and ultimately behavior. One neuromodulator, dopamine, has been studied extensively in its role as reward signal during learning and memory across animal species. Newer evidence suggests that dopaminergic neurons (DANs) can modulate sensory perception acutely, thereby allowing an animal to adapt its behavior and decision-making to its internal and behavioral state. In addition, some data indicate that DANs are heterogeneous and convey different types of information as a population. We have investigated DAN population activity and how it could encode relevant information about sensory stimuli and state by taking advantage of the confined anatomy of DANs innervating the mushroom body (MB) of the fly <jats:italic>Drosophila melanogaster</jats:italic>. Using <jats:italic>in vivo</jats:italic> calcium imaging and a custom 3D image registration method, we find that the activity of the population of MB DANs is predictive of the innate valence of an odor as well as the metabolic and mating state of the animal. Furthermore, DAN population activity is strongly correlated with walking or running, consistent with a role of dopamine in conveying behavioral state to the MB. Together our data and analysis suggest that distinct DAN population activities encode innate odor valence, movement and physiological state in a MB-compartment specific manner. We propose that dopamine shapes innate odor perception through combinatorial population coding of sensory valence, physiological and behavioral context.</jats:p>

Modulation of flight and feeding behaviours requires presynaptic IP3Rs in dopaminergic neurons

“…In neurons expressing IP 3 R DN and GCaMP optogenetic stimulation of CsChrimsom did not evince a significant Ca 2+ response either during or after the red light stimulus, as compared with the control genotype expressing RFP and GCaMP ( Figure 6A,B and Figure 6—source data 1 ). In agreement with recent findings, some MB296B neurons exhibit high basal activity even in the absence of optogenetic stimulation ( Figure 6—figure supplement 1 ; Siju et al, 2020 ). Similar results were obtained by KCl - evoked depolarisation in the presence of 2 μM Tetrodotoxin (TTX) ( Figure 6—figure supplement 1A,B , Figure 6—source data 3 ).…”

Circuits for integrating learned and innate valences in the insect brain

“…High variability in MBON responses to odor across individuals has previously also been observed in the adult flies and has been related to different individual experiences [30]. The MBs can also compute other kinds of information, such as internal state [78][79][80][81][82][83] which may modulate an individual's disposition towards sensory stimuli. Therefore, the average response across untrained individuals might be similar to the response of a single individual in a naive neutral state (with any interindividual differences averaged out across a population), and the variability may represent the degree of freedom for the MB to tune this response to a stimulus depending on previous experience or state.…”

A neural circuit architecture for rapid behavioral flexibility in goal-directed navigation

“…A prime candidate for such a role is the ventral FB dopaminergic neuron (DAN) type. MB DANs are known to carry reinforcement (and movement) signals and be involved in associative learning in that brain region [119][120][121][122][123], and a subset of FB DANs -potentially the ventral FB DANs, such as FB2A, FB4L or FB4M, rather than the dorsal FB DANs that have been associated with sleep-and nutrient-related signaling-may well perform similar functions. Interestingly, most tangential neurons that innervate the ventral FB receive local input from columnar FB neurons -including subtypes of PFN, PFR, v∆ and h∆ neurons-near their presynaptic sites in the FB [34], suggesting that any reinforcement signals they might carry would likely be locally shaped by heading input, as required by our model.…”