We study how aversive experiences trigger alterations in brain circuits and neural coding resulting in emotional memory formation.

Joshua Johansen

Joshua Johansen, Ph.D.

Team Leader, Neural Circuitry of Learning and Memory
joshua.johansen [at] riken.jp

Research Overview

Our experiences in the world produce physical changes in the brain and as a result of these changes memories are formed. However, in our daily lives we are constantly barraged by sensory information, most of which we do not remember. What tells the brain to store some experiences as memories while others are forgotten? Answering this question is a central goal of our laboratory.
Pleasurable and aversive experiences are powerful triggers for memory storage, telling our brain when an experience should be stored and remembered. To accomplish this task, aversive and pleasurable encounters activate neural 'teaching signal' circuits which can trigger brain alterations resulting in memory formation. Relative to our understanding of sensory and motor circuits, we understand very little about the brain circuits and mechanisms which translate aversive experiences into neural teaching signals.
Though we are generally interested in the neural circuit mechanisms of associative learning and memory, our laboratory focuses on the study of teaching signals by examining the neural processes by which aversive experiences trigger behavioral fear conditioning. We study teaching signals using fear conditioning, a powerful model for studying behavioral memory formation. We take advantage of a multi-disciplinary approach, employing state of the art optogenetic techniques to causally manipulate teaching signal circuits and in-vivo electrophysiological methods to examine the computations performed by neurons in these circuits during behavioral learning. Our goals are to define the circuits that trigger aversive memory formation and elucidate the mechanisms by which aversive experiences trigger neural plasticity in memory storage areas. In addition, we aim to determine the computations performed by neurons in different parts of these circuits and establish how circuit processes give rise to these neural computations during behavioral learning and memory. Using this strategy we ultimately seek to discover general principles of neural circuit function, neural coding and plasticity as they relate to adaptive behavior.


Selected Publications

  1. Yeh LF, Ozawa T, Johansen JP
    "Functional organization of the midbrain periaqueductal gray for regulating aversive memory formation"
    Molecular Brain, 14, 136 (2021)
  2. Likhtik E, Johansen JP
    "Neuromodulation in Circuits of Aversive Emotional Learning"
    Nature Neuroscience, Nov;22(11):1946 (2019)
  3. Luo R, Uematsu A, Weitemier A, Aquili L, Koivumaa J, McHugh TJ, Johansen JP
    "A dopaminergic switch for fear to safety transitions"
    Nature Communications, 2483 (2018)
  4. Yeh L-F, Watanabe M, Sulkes-Cuevas J, Johansen JP
    "Dysregulation of aversive signaling pathways: a novel circuit endophenotype for pain and anxiety disorders"
    Current Opinion in Neurobiology, 48:37-44 (2017)
  5. Uematsu A, Tan BZ, Ycu EA, Sulkes-Cuevas J, Koivumaa J, Junyent F, Kremer EJ, Witten IB, Deisseroth K, Johansen JP
    "Modular organization of the brainstem noradrenaline system coordinates opposing learning states"
    Nature Neuroscience, Advance Online Publication (2017)
    - Featured in Nature Neuroscience News & Views 20(11), 1517-1519 (2017)
  6. Ozawa T, Ycu EA, Kumar A, Yeh L-F, Ahmed T, Koivumaa J, Johansen JP
    "A feedback neural circuit for calibrating aversive memory strength"
    Nature Neuroscience, 20(1):90-97 (2017)
  7. Madarasz TJ, Diaz-Mataix L Akhand O, Ycu EA, LeDoux JE, Johansen JP
    "Evaluation of ambiguous associations in the amygdala by learning the structure of the environment"
    Nature Neuroscience, 19:965-972 (2016)
  8. Herry C, Johansen JP
    "Encoding of fear learning and memory in distributed neuronal circuits"
    Nature Neuroscience, 17(12):1644-54 (2014)
  9. Johansen JP
    "Neuroscience: Anxiety is the sum of its parts"
    Nature, 496(7444):174-5 (2013)
  10. Johansen JP, Tarpley JW, LeDoux JE, Blair HT
    "Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray"
    Nature Neuroscience, 13(8):979-86 (2010)

Lab Members

Principal investigator

Joshua Johansen
Laboratory Head

Core members

Xiaowei Gu
Research Scientist
Tomoya Ohnuki
Postdoctoral Researcher
Mehdi Julien Sicre
Postdoctoral Researcher
Nur Zeynep Gungor
Special Postdoctoral Researcher
Mayumi Watanabe
Research Associate
Jessica Natali Sulkes Cuevas
Research Associate
Li-Feng Yeh
Research Associate
Yusuke Kasuga
Research Associate
Yuri Ishizu
Technical Staff I
Reiko Yoshida
Technical Staff I
Yuki Goya
Technical Staff I