Dana Shani Galili1, Kristina V Dylla2, Alja Lüdke2, Anja B Friedrich1, Nobuhiro Yamagata3, Jin Yan Hilary Wong1, Chien Hsien Ho1, Paul Szyszka2, Hiromu Tanimoto4. 1. Max-Planck-Institut für Neurobiologie, Am Klopferspitz 18, 82152 Martinsried, Germany. 2. Department of Biology-Neurobiology, University of Konstanz, 78457 Konstanz, Germany. 3. Graduate School of Life Sciences, Tohoku University, Katahira 2-1-1, 980-8577 Sendai, Japan. 4. Max-Planck-Institut für Neurobiologie, Am Klopferspitz 18, 82152 Martinsried, Germany; Graduate School of Life Sciences, Tohoku University, Katahira 2-1-1, 980-8577 Sendai, Japan. Electronic address: hiromut@m.tohoku.ac.jp.
Abstract
BACKGROUND: Drosophila learn to avoid odors that are paired with aversive stimuli. Electric shock is a potent aversive stimulus that acts via dopamine neurons to elicit avoidance of the associated odor. While dopamine signaling has been demonstrated to mediate olfactory electric shock conditioning, it remains unclear how this pathway is involved in other types of behavioral reinforcement, such as in learned avoidance of odors paired with increased temperature. RESULTS: To better understand the neural mechanisms of distinct aversive reinforcement signals, we here established an olfactory temperature conditioning assay comparable to olfactory electric shock conditioning. We show that the AC neurons, which are internal thermal receptors expressing dTrpA1, are selectively required for odor-temperature but not for odor-shock memory. Furthermore, these separate sensory pathways for increased temperature and shock converge onto overlapping populations of dopamine neurons that signal aversive reinforcement. Temperature conditioning appears to require a subset of the dopamine neurons required for electric shock conditioning. CONCLUSIONS: We conclude that dopamine neurons integrate different noxious signals into a general aversive reinforcement pathway.
BACKGROUND:Drosophila learn to avoid odors that are paired with aversive stimuli. Electric shock is a potent aversive stimulus that acts via dopamine neurons to elicit avoidance of the associated odor. While dopamine signaling has been demonstrated to mediate olfactory electric shock conditioning, it remains unclear how this pathway is involved in other types of behavioral reinforcement, such as in learned avoidance of odors paired with increased temperature. RESULTS: To better understand the neural mechanisms of distinct aversive reinforcement signals, we here established an olfactory temperature conditioning assay comparable to olfactory electric shock conditioning. We show that the AC neurons, which are internal thermal receptors expressing dTrpA1, are selectively required for odor-temperature but not for odor-shock memory. Furthermore, these separate sensory pathways for increased temperature and shock converge onto overlapping populations of dopamine neurons that signal aversive reinforcement. Temperature conditioning appears to require a subset of the dopamine neurons required for electric shock conditioning. CONCLUSIONS: We conclude that dopamine neurons integrate different noxious signals into a general aversive reinforcement pathway.
Authors: Nobuhiro Yamagata; Toshiharu Ichinose; Yoshinori Aso; Pierre-Yves Plaçais; Anja B Friedrich; Richard J Sima; Thomas Preat; Gerald M Rubin; Hiromu Tanimoto Journal: Proc Natl Acad Sci U S A Date: 2014-12-29 Impact factor: 11.205
Authors: Daisuke Hattori; Yoshinori Aso; Kurtis J Swartz; Gerald M Rubin; L F Abbott; Richard Axel Journal: Cell Date: 2017-05-11 Impact factor: 41.582
Authors: Katharina Eichler; Feng Li; Ashok Litwin-Kumar; Youngser Park; Ingrid Andrade; Casey M Schneider-Mizell; Timo Saumweber; Annina Huser; Claire Eschbach; Bertram Gerber; Richard D Fetter; James W Truman; Carey E Priebe; L F Abbott; Andreas S Thum; Marta Zlatic; Albert Cardona Journal: Nature Date: 2017-08-09 Impact factor: 49.962