Temperature representation in the Drosophila brain.
In Drosophila, rapid temperature changes are detected at the periphery by dedicated receptors forming a simple sensory map for hot and cold in the brain. However, flies show a host of complex innate and learned responses to temperature, indicating that they are able to extract a range of information from this simple input. Here we define the anatomical and physiological repertoire for temperature representation in the Drosophila brain. First, we use a photolabelling strategy to trace the connections that relay peripheral thermosensory information to higher brain centres, and show that they largely converge onto three target regions: the mushroom body, the lateral horn (both of which are well known centres for sensory processing) and the posterior lateral protocerebrum, a region we now define as a major site of thermosensory representation. Next, using in vivo calcium imaging, we describe the thermosensory projection neurons selectively activated by hot or cold stimuli. Fast-adapting neurons display transient ON and OFF responses and track rapid temperature shifts remarkably well, while slow-adapting cell responses better reflect the magnitude of simple thermal changes. Unexpectedly, we also find a population of broadly tuned cells that respond to both heating and cooling, and show that they are required for normal behavioural avoidance of both hot and cold in a simple two-choice temperature preference assay. Taken together, our results uncover a coordinated ensemble of neural responses to temperature in the Drosophila brain, demonstrate that a broadly tuned thermal line contributes to rapid avoidance behaviour, and illustrate how stimulus quality, temporal structure, and intensity can be extracted from a simple glomerular map at a single synaptic station.
Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA.
Dominic D
DD
Frank
Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA.
Genevieve C
GC
Jouandet
Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA.
Patrick J
PJ
Kearney
Departments of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA.
Lindsey J
LJ
Macpherson
Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA.
Marco
M
Gallio
D000818:Animals; D001921:Brain / Q000033:anatomy & histology / Q000166:cytology / Q000502:physiology*; D001931:Brain Mapping; D002118:Calcium / Q000032:analysis / Q000378:metabolism; D004331:Drosophila melanogaster / Q000166:cytology / Q000502:physiology*; D024521:Mushroom Bodies / Q000294:innervation; D009434:Neural Pathways; D009474:Neurons / Q000378:metabolism; D013569:Synapses / Q000378:metabolism; D013696:Temperature; D013823:Thermoreceptors / Q000378:metabolism; D013697:Thermosensing / Q000502:physiology*; D013997:Time Factors
D002118:Calcium