A rise-to-threshold signal for a relative value deliberation

Abstract

Whereas progress has been made in identifying neural signals related to rapid, cued decisions, less is known about how brains guide and terminate more ethologically relevant deliberations, where an animal's own behavior governs the options experienced over minutes. Drosophila search for many seconds to minutes for egg-laying sites with high relative value and neurons, called oviDNs, exist whose activity fulfills necessity and sufficiency criteria for initiating the egg-deposition motor program. Here we show that oviDNs express a calcium signal that rises over seconds to minutes as a fly deliberates whether to lay an egg. The calcium signal dips when an egg is internally prepared (ovulated), rises at a rate related to the relative value of the current substrate being experienced, and reaches a consistent peak just prior to the abdomen bend for egg deposition. We provide perturbational evidence that the egg-deposition motor program is initiated once this signal hits a threshold and that sub-threshold variation in the signal regulates the time spent deliberating and, ultimately, the option chosen. These results argue that a rise-to-threshold signal guides Drosophila to lay eggs on substrate options with high relative value, with each egg-laying event representing a self-paced decision similar to real-world decisions made by humans and other mammals.

A functional division of Drosophila sweet taste neurons that is value-based and task-specific

“…Second, converting different sensory cues (e.g., sweetness and firmness) associated with an option into value-modifying signals may allow options of disparate properties to be compared directly via a so-called “common currency.” Third, having sweetness engage a value-modifying circuit may allow animals more flexibility in adjusting the value of a sweet option according to decision contexts. For example, while flies prefer the plain option in certain two-choice contexts ( 31 , 32 , 48 ), they prefer the sweet option when laying eggs in a significantly larger enclosure ( 49 ). Perhaps larger enclosures promote sweet preference either by enhancing the output of the value-increasing pathway potentially mediated by the labellar sweet neurons or by dampening the value-decreasing one mediated by the leg sweet neurons.…”

“…While egg-laying preference has been frequently used for studying the function of different sensory systems ( 24 , 50 – 61 ), the central circuit that assigns, retains, and compares values of egg-laying options has yet to be elucidated. Two recent studies suggest that the descending egg-laying command neurons (oviDNs) must be an integral component of the decision circuit as they not only are capable of triggering egg-laying when directly activated but also express a [Ca 2+ ] signal that tracks the relative value of an egg-laying option ( 33 , 48 ). On the other hand, while successful rejection of the otherwise acceptable sweet option in the sweet versus plain task requires that the animals hold in memory their recent encounters with the preferred plain option, our previous studies have ruled out a critical role of the learning-and-memory center mushroom bodies in this decision ( 32 ).…”

Evolutionary divergence in sugar valuation shifts Drosophila suzukii oviposition choice towards ripe fruit

“…Recent data suggests that the oviDN neurons act as a temporal accumulator of sensory and internal drive for oviposition and enact the decision to lay an egg upon reaching a specific threshold of activity. The rate at which activity rises in oviDN neurons appears to encode substrate attractivity for oviposition 50 . This raises the exciting hypothesis that inter-species divergent sugar valuation could arise from physiological differences in oviposition circuits affecting the rate of activity rising or threshold height required in oviDN neurons to trigger oviposition in response to sugar stimulation ( Fig.…”

An internal expectation guides Drosophila egg-laying decisions

“…1A and fig. S1A) (16). The 2.5-mm barrier is approximately the length of the fly, which means that the fly's legs touched either one substrate or the other, but rarely (if ever) touched both substrates at the same time.…”

“…First, because flies cannot see or smell sucrose at a distance, if flies changed their egg-laying rate on one sucrose substrate due to the existence of a second, we could be sure that this was due to a historical effect of experiencing the second substrate and not due to them currently sensing the distant substrate. Second, previous work has extensively demonstrated that flies make a relative comparison between two sucrose-containing substrates (8,9,16). That is, if flies are only allowed to lay eggs on 0, 200, or 500 mM sucrose substrates, all are acceptable; however, when flies are allowed to choose between any pair of such options, they strongly prefer the lower concentration (schematized in Fig.…”