Innate preference toward environmental conditions is crucial for animal survival. Although much is known about the neural processing of sensory information, how the aversive or attractive sensory stimulus is transformed through central brain neurons into avoidance or approaching behavior is largely unclear. Here we show that Drosophila larval light preference behavior is regulated by a disinhibitory mechanism. In the disinhibitory circuit, a pair of GABAergic neurons exerts tonic inhibition on one pair of contralateral projecting neurons that control larval reorientation behavior. When a larva enters the light area, the reorientation-controlling neurons are disinhibited to allow reorientation to occur as the upstream inhibitory neurons are repressed by light. When the larva exits the light area, the inhibition on the downstream neurons is restored to repress further reorientation and thus prevents the larva from re-entering the light area. We suggest that disinhibition may serve as a common neural mechanism for animal innate preference behavior.

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Drosophila larvae exhibit klinotaxis when placed in a gradient of temperature, chemicals, or light. The larva samples environmental stimuli by casting its head from side to side. By comparing the results of two consecutive samples, it decides the direction of movement, appearing as a turn proceeded by one or more head casts. Here by analyzing larval behavior in a light-spot-based phototaxis assay, we showed that, in addition to turns with a single cast (1-cast), turns with multiple head casts (n-cast) helped to improve the success of light avoidance. Upon entering the light spot, the probability of escape from light after the first head cast was only ~30%. As the number of head casts increased, the chance of successful light avoidance increased and the overall chance of escaping from light increased to >70%. The amplitudes of first head casts that failed in light avoidance were significantly smaller in n-cast turns than those in 1-cast events, indicating that n-cast turns might be planned before completion of the first head cast. In n-casts, the amplitude of the second head cast was generally larger than that of the first head cast, suggesting that larvae tried harder in later attempts to improve the efficacy of light avoidance. We propose that both 1-cast turns and n-cast turns contribute to successful larval light avoidance, and both can be initiated at the first head cast.

Animal’s innate avoidance behavior is crucial for its survival. It subjects to modulation by environmental conditions in addition to the commanding sensorimotor transformation pathway. Although much has been known about the commanding neural basis, relatively less is known about how innate avoidance behavior is shaped by external conditions. Here in this paper, we report that Drosophila larvae showed stronger light avoidance at lower temperatures than at higher temperatures. Such negative regulation of light avoidance by temperature was abolished by blocking two pairs of central brain neurons, ACLPR60F09 neurons, that were responsive to both light and temperature change, including cooling and warming. ACLPR60F09 neurons could be excited by pdf-LaN neurons in the visual pathway. On the downstream side, they could inhibit the CLPNR82B09 neurons that command light induced reorientation behavior. Compared with at warm temperature, ACLPR60F09 neurons’ response to light was decreased at cool temperature so that the inhibition on CLPNR82B09 neurons was relieved and the light induced avoidance was enhanced. Our result proposed a neural mechanism underlying cross-modal modulation of animal innate avoidance behavior.

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