Behavioural choice emerges from nonlinear all-to-all interactions between drives

Abstract

Under the right conditions any drive can overcome nearly any other, yet studies of 1 behavioural selection predominantly focus on only one, or occasionally two behaviours. 2We present an experimental and computational framework that captures and explains the 3 resolution of conflicts between several competing motivations. We characterize neurons 4 that integrate information from all rival drives to generate an aggregate signal that urges 5 male Drosophila to transition out of mating. Experimental investigation of these Drive 6 Integrating Neurons (DINs) revealed time-varying, supralinear interactions among 7 competing drives that stimulate the DINs and induce a change in behaviour. Extending 8 these findings to model the interactions between all of an animal's motivations led to the 9 surprising prediction that, under many conditions, all-to-all interactions actually buffer 10 the dominant drive against challengers. We experimentally validated this prediction, 11 showing that weak drives for a variety of tertiary goals can have a profound stabilizing 12 effect on the ongoing behaviour. These results emerge only if non-linear integration of 13 other motivations occurs for each of an animal's drives, suggesting the potential 14 universality of this mechanism. Our findings emphasize the interconnectedness of 15 motivational systems and the consequent importance of considering the full motivational 16 state of an animal to understand its behaviour. 17 18 INTRODUCTION 19 Animals often have multiple unmet needs, and attempting to satisfy one generally precludes 20 pursuing the others 1 . No one drive is strictly dominant; under the right conditions the pursuit of 21 nearly any goal may be suppressed by another 2 . At some level behaviour-specific drive states 22 must therefore affect the circuitry underlying many other behaviours 3 , and this information must 23 be integrated to arrive at a consensus. The ethologist Konrad Lorenz used the metaphor of a 24 "great parliament of instincts" to describe the behaviour of animals 2 , and the philosopher and 25 mathematician Bertrand Russell noted in his Nobel Prize acceptance speech that "If you wish to 26 know what men [sic] will do, you must know…the whole system of their desires with their 27 relative strengths" 4 . Nearly all studies on the interactions between competing motivations, in 28contrast, focus on the resolution between just two drives in conflict. Here we establish an 29 experimental and computational framework for examining the many interactions between 30 simultaneous drive states that must be considered to understand naturalistic decision-making. 32The mating duration of Drosophila melanogaster provides a clear and quantitative readout of the 33 interplay between competing drives: to switch behaviours the male must first terminate the 34 mating. If undisturbed, copulation will last ~23 minutes; if a dangerous situation arises, the male 35 may truncate the mating to flee, depending on both the severity of the threat and how far the 36 mating has progressed 5 ...

Local desensitization to dopamine devalues recurring behavior

“…A strong candidate for receiving the signal through the D2R is a set of eight GABAergic Copulation Decision Neurons (CDNs, labeled by NP2719-Gal4), that reside in the abdominal ganglion, in close proximity to dopaminergic neurons (Figure 2B) 17 . As expected from neurons that mediate the decision to end matings 17,20 , electrical silencing of the CDNs suppressed the increased termination caused by electrical silencing of dopamine neurons (Supplementary Figure 4C). We found that rescuing D2R expression only in the CDNs of D2R mutant animals restored normal threat resiliency (Figure 2C, Supplementary Figure 4D), without causing an increase in baseline (i.e., first mating) persistence (Supplementary Figure 4E).…”

“…For the first five minutes of a ∼23-minute mating, male flies demonstrate an apparently insurmountable motivation to persist in the face of even lethal challenges 17,33 . As the mating progresses their resiliency declines, such that by 15 minutes even relatively modest environmental changes can truncate most matings 17,20 . If supplied with an abundance of females and left to mate ad libitum , males will mate multiple times, depleting their reserves of reproductive fluid after 3-5 matings and rendering future matings unproductive 6,34 .…”

“…If supplied with an abundance of females and left to mate ad libitum , males will mate multiple times, depleting their reserves of reproductive fluid after 3-5 matings and rendering future matings unproductive 6,34 . Though courtship decreases after each mating ( Supplementary Figure 1A ), even completely satiated males will still occasionally court and mate 18 , allowing us to ask whether these unproductive matings are guided by the same motivational dynamics as productive ones 17,20 . We found that, after spending 2.5 hours mating ad libitum with females in a satiety assay (1 male with ∼15 virgin females 6,34 ; see Methods ), males become much more likely to terminate subsequent matings when challenged ( Figure 1A, B, Supplementary Figure 1B ).…”

“…We first confirmed that electrical silencing of the CDNs prevented satiated males from ending matings in response to a heat threat at 8 minutes ( Supplementary Figure 6A ), consistent with their role as arbiters of the decision-making process. Optogenetic stimulation of the CDNs causes mating termination with probabilities that depend on stimulation duration and intensity, as well as the time into mating when the stimulus is delivered 17,20 (Gautham et al, in revision). While basal activity of the CDNs was unchanged ( Supplementary Figure 6B ), we found that prior matings increased the ability of optogenetic CDN stimulation to terminate matings over a range of light intensities, with a magnitude comparable to heat threats ( Supplementary Figure 6C, D ).…”

“…But subjecting the male to threats at varying times into mating reveals an increasing susceptibility to abandonment later into mating 17 . Local dopamine signaling counters challenges to mating by dampening the output of the Copulation Decision Neurons (CDNs), whose activity is required to end matings 17,20 . We show that the mating-protective influence of dopamine is conveyed directly to the CDNs through the D2 receptor, an effect that both protects the current mating and desensitizes the receptor for future matings.…”