A single pair of interneurons commands the Drosophila feeding motor program

• Published in: Nature (London) Vol. 499; no. 7456; pp. 83 - 87
• Main Authors: Flood, Thomas F., Iguchi, Shinya, Gorczyca, Michael, White, Benjamin, Ito, Kei, Yoshihara, Motojiro
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 04.07.2013; Nature Publishing Group
• Subjects: 631/378/1595/1395; 631/378/2591; 631/443/376; 631/601/18; Amphibia; Animals; Biological and medical sciences; Brain - cytology; Brain - physiology; Calcium Signaling; Carbohydrates; Cues; Decision Making - physiology; Drosophila; Drosophila melanogaster - genetics; Drosophila melanogaster - physiology; Electrophysiology; Feeding behavior; Feeding Behavior - physiology; Female; Food; Food and nutrition; Food Deprivation; Fundamental and applied biological sciences. Psychology; Glass substrates; Humanities and Social Sciences; Insects; Interneurons; Interneurons - cytology; Interneurons - physiology; letter; Male; Models, Neurological; Movement - physiology; multidisciplinary; Neurons; Pharynx - physiology; Physiological aspects; Psychomotor Performance - physiology; Reflex; Science; Sucrose; Sugar; Temperature; Toads; Vertebrates: nervous system and sense organs; United States; Human; Feeding behavior; Calcium; Central nervous system; Electrophysiology; Nervous system; Motor neuron; Ablation; Feeding; Encephalon; Interneuron; Characterization; Imaging
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature12208

A pair of Drosophila brain cells is identified and its activation alone is found to induce the fly’s complete feeding motor routine when artificially induced; suppressing or ablating these two neurons eliminates the sugar-induced feeding behaviour, but ablation of just one neuron results in asymmetric movements. Eating behaviour controlled by just two neurons How much redundancy there is in the nervous system is still an open question. Now Motojiro Yoshihara and colleagues have identified a pair of Drosophila brain cells, which they name 'feeding' (Fdg) neurons, whose artificial activation is sufficient to induce the fly's complete feeding motor routine. The suppression or ablation of just these two neurons eliminates the sugar-induced feeding reflex, but ablation of just one of them results in asymmetric movements. This work reveals a severe bottleneck in the coupling of sensory, metabolic and motor systems. Many feeding behaviours are the result of stereotyped, organized sequences of motor patterns. These patterns have been the subject of neuroethological studies 1 , 2 , such as electrophysiological characterization of neurons governing prey capture in toads 1 , 3 . However, technical limitations have prevented detailed study of the functional role of these neurons, a common problem for vertebrate organisms. Complexities involved in studies of whole-animal behaviour can be resolved in Drosophila, in which remote activation of brain cells by genetic means 4 enables us to examine the nervous system in freely moving animals to identify neurons that govern a specific behaviour, and then to repeatedly target and manipulate these neurons to characterize their function. Here we show neurons that generate the feeding motor program in Drosophila . We carried out an unbiased screen using remote neuronal activation and identified a critical pair of brain cells that induces the entire feeding sequence when activated. These ‘feeding neurons’ (here abbreviated to Fdg neurons for brevity) are also essential for normal feeding as their suppression or ablation eliminates sugar-induced feeding behaviour. Activation of a single Fdg neuron induces asymmetric feeding behaviour and ablation of a single Fdg neuron distorts the sugar-induced feeding behaviour to become asymmetric, indicating the direct role of these neurons in shaping motor-program execution. Furthermore, recording neuronal activity and calcium imaging simultaneously during feeding behaviour 5 reveals that the Fdg neurons respond to food presentation, but only in starved flies. Our results demonstrate that Fdg neurons operate firmly within the sensorimotor watershed, downstream of sensory and metabolic cues and at the top of the feeding motor hierarchy, to execute the decision to feed.