A rise-to-threshold process for a relative-value decision

• Published in: Nature (London) Vol. 619; no. 7970; pp. 563 - 571
• Main Authors: Vijayan, Vikram, Wang, Fei, Wang, Kaiyu, Chakravorty, Arun, Adachi, Atsuko, Akhlaghpour, Hessameddin, Dickson, Barry J., Maimon, Gaby
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 20.07.2023
• Subjects: 13/51; 14; 14/19; 14/69; 631/378/2629/1409; 631/378/2649/1409; 64; 64/24; 9/74; Animals; Calcium Signaling; Decision Making - physiology; Drosophila melanogaster - anatomy & histology; Drosophila melanogaster - physiology; Female; Humanities and Social Sciences; multidisciplinary; Neural Pathways; Neurons - metabolism; Oviposition - physiology; Presynaptic Terminals - metabolism; Psychomotor Performance; Science; Science (multidisciplinary)
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/s41586-023-06271-6

Whereas progress has been made in the identification of neural signals related to rapid, cued decisions 1 – 3 , less is known about how brains guide and terminate more ethologically relevant decisions in which an animal’s own behaviour governs the options experienced over minutes 4 – 6 . Drosophila search for many seconds to minutes for egg-laying sites with high relative value 7 , 8 and have neurons, called oviDNs, whose activity fulfills necessity and sufficiency criteria for initiating the egg-deposition motor programme 9 . Here we show that oviDNs express a calcium signal that (1) dips when an egg is internally prepared (ovulated), (2) drifts up and down over seconds to minutes—in a manner influenced by the relative value of substrates—as a fly determines whether to lay an egg and (3) reaches a consistent peak level just before the abdomen bend for egg deposition. This signal is apparent in the cell bodies of oviDNs in the brain and it probably reflects a behaviourally relevant rise-to-threshold process in the ventral nerve cord, where the synaptic terminals of oviDNs are located and where their output can influence behaviour. We provide perturbational evidence that the egg-deposition motor programme is initiated once this process hits a threshold and that subthreshold variation in this process regulates the time spent considering options and, ultimately, the choice taken. Finally, we identify a small recurrent circuit that feeds into oviDNs and show that activity in each of its constituent cell types is required for laying an egg. These results argue that a rise-to-threshold process regulates a relative-value, self-paced decision and provide initial insight into the underlying circuit mechanism for building this process. The Drosophila egg-deposition motor programme is initiated once a rise-to-threshold process hits a threshold, and subthreshold variation in this process regulates the time spent considering options.