A Circuit Encoding Absolute Cold Temperature in Drosophila

Animals react to environmental changes over timescales ranging from seconds to days and weeks. An important question is how sensory stimuli are parsed into neural signals operating over such diverse temporal scales. Here, we uncover a specialized circuit, from sensory neurons to higher brain centers, that processes information about long-lasting, absolute cold temperature in Drosophila. We identify second-order thermosensory projection neurons (TPN-IIs) exhibiting sustained firing that scales with absolute temperature. Strikingly, this activity only appears below the species-specific, preferred temperature for D. melanogaster (∼25°C). We trace the inputs and outputs of TPN-IIs and find that they are embedded in a cold “thermometer” circuit that provides powerful and persistent inhibition to brain centers involved in regulating sleep and activity. Our results demonstrate that the fly nervous system selectively encodes and relays absolute temperature information and illustrate a sensory mechanism that allows animals to adapt behavior specifically to cold conditions on the timescale of hours to days. [Display omitted] •The fly antenna contains 3 types of cold-activated sensory neurons•Cold cells converge on “cold” domain of the brain thermosensory map•Second-order TPN-IIs relay absolute cold, below D. melanogaster’s favorite 25°C•TPN-IIs inhibit DN1a circadian neurons, adapting sleep to cold/dark conditions Alpert et al. uncover a specialized circuit, from sensory neurons to higher brain centers that processes information about absolute cold temperature in Drosophila. This circuit directly connects thermosensory neurons of the antenna with circadian and sleep centers in the brain, adapting sleep and activity specifically to cold conditions.