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 ...

7Computations in the brain are broadly assumed to emerge from patterns of fast electrical 8 activity. Challenging this view, we show that a male fly's decision to persist in mating, 9 even through a potentially lethal threat, hinges on biochemical computations that enable 10 processing over minutes to hours. Each neuron in a recurrent network measuring time 11 into mating contains slightly different internal molecular estimates of elapsed time. 12Protein Kinase A (PKA) activity contrasts this internal measurement with input from the 13 other neurons to represent evidence that the network's goal has been achieved. When 14 consensus is reached, PKA pushes the network toward a large-scale and synchronized 15 burst of calcium influx, which we call an eruption. The eruption functions like an action 16 potential at the level of the network, transforming deliberation within the network into an 17 all-or-nothing output, after which the male will no longer sacrifice his life to continue 18 mating. We detail the continuous transformation between interwoven molecular and 19 electrical information over long timescales in this system, showing how biochemical 20 activity, invisible to most large scale recording techniques, is the key computational 21 currency directing a life-or-death decision. 22 23 24 25 32 33A fundamental problem in neural computation stems from the need for neurons within a 34 network to communicate without triggering premature responses in downstream 35 circuitry 1-3 . This problem is compounded when the computations are performed over 36 long timescales, as in many decision-making paradigms 4 . In single neurons, the action 37 potential solves an analogous problem by transforming accumulated positive and 38 negative inputs into a transient, all-or-nothing output that is broadcasted to postsynaptic 39 targets. Here we identify a similar mechanism acting at the network level and over 40 timescales ranging from seconds to hours, which we call an eruption. 42The Corazonin-expressing (Crz) neurons of the male abdominal ganglion comprise an 43 exceptionally tractable system for investigating neuronal networks and behavioral 44 control. These four neurons drive two simultaneous and crucial events in the lives of the 45 male and his mating partner: i) the transfer of sperm from the male to the female 5 and ii) 46 a transition out of a period of insurmountably high motivation to continue mating 6 . Both of 47 these events occur six minutes after a mating begins and are under the control of a 48 molecular timer encoded by the slowly-decaying autophosphorylation of the kinase 49 CaMKII 6 . We show that the Crz neurons use cyclic AMP (cAMP) signaling to average 50 evidence about the passage of time across the network and generate an eruption that 51 signals to downstream circuitry only when a consensus is reached. In addition to 52 revealing a new network phenomenon, these results explain the function of CaMKII in 53 the only mechanism for interval timing yet to be described. 55 RESULTS 57The Crz neurons form a recu...