Current understanding of fear learning and memory in humans and animal models and the value of a linguistic approach for analyzing fear learning and memory in humans

Jacob Raber; Shahar Arzy; Julie Boulanger Bertolus; Brendan Depue; Haley E Haas; Stefan G Hofmann; Maria Kangas; Elizabeth Kensinger; Christopher A Lowry; Hilary A Marusak; Jessica Minnier; Anne-Marie Mouly; Andreas Mühlberger; Seth Davin Norrholm; Kirsi Peltonen; Graziano Pinna; Christine Rabinak; Youssef Shiban; Hermona Soreq; Michael A van der Kooij; Leroy Lowe; Leah T Weingast; Paula Yamashita; Sydney Weber Boutros

doi:10.1016/j.neubiorev.2019.03.015

Current understanding of fear learning and memory in humans and animal models and the value of a linguistic approach for analyzing fear learning and memory in humans

Neurosci Biobehav Rev. 2019 Oct:105:136-177. doi: 10.1016/j.neubiorev.2019.03.015. Epub 2019 Apr 7.

Authors

Jacob Raber¹, Shahar Arzy², Julie Boulanger Bertolus³, Brendan Depue⁴, Haley E Haas⁵, Stefan G Hofmann⁶, Maria Kangas⁷, Elizabeth Kensinger⁸, Christopher A Lowry⁹, Hilary A Marusak¹⁰, Jessica Minnier¹¹, Anne-Marie Mouly³, Andreas Mühlberger¹², Seth Davin Norrholm⁵, Kirsi Peltonen¹³, Graziano Pinna¹⁴, Christine Rabinak¹⁰, Youssef Shiban¹², Hermona Soreq¹⁵, Michael A van der Kooij¹⁶, Leroy Lowe¹⁷, Leah T Weingast⁵, Paula Yamashita¹¹, Sydney Weber Boutros¹⁸

Affiliations

¹ Department of Behavioral Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA; Departments of Neurology and Radiation Medicine, and Division of Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA. Electronic address: raberj@ohsu.edu.
² Department of Medical Neurobiology, Hebrew University, Jerusalem 91904, Israel.
³ Lyon Neuroscience Research Center, CNRS-UMR 5292, INSERM U1028, Université Lyon, Lyon, France.
⁴ Departments of Psychological and Brain Sciences and Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, USA.
⁵ Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, GA, USA.
⁶ Department of Psychological and Brain Sciences, Boston University, Boston, MA, USA.
⁷ Department of Psychology, Macquarie University, Sydney, Australia.
⁸ Department of Psychology, Boston College, Boston, MA, USA.
⁹ Department of Integrative Physiology and Center for Neuroscience, University of Colorado Boulder, Boulder, CO, USA.
¹⁰ Department of Pharmacy Practice, Wayne State University, Detroit, MI, USA.
¹¹ School of Public Health, Oregon Health & Science University, Portland, OR, USA.
¹² Department of Psychology (Clinical Psychology and Psychotherapy), University of Regensburg, Regensburg, Germany; PFH - Private University of Applied Sciences, Department of Psychology (Clinical Psychology and Psychotherapy Research), Göttingen, Germany.
¹³ Faculty of Social Sciences/Psychology, Tampere University, Tampere, Finland.
¹⁴ The Psychiatric Institute, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
¹⁵ Department of Biological Chemistry, Edmond and Lily Safra Center of Brain Science and The Institute of Life Sciences, Hebrew University, Jerusalem 91904, Israel.
¹⁶ Translational Psychiatry, Department of Psychiatry and Psychotherapy, Universitatsmedizin der Johannes Guttenberg University Medical Center, Mainz, Germany.
¹⁷ Neuroqualia, Nova Scotia, Canada.
¹⁸ Department of Behavioral Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA.

PMID: 30970272
DOI: 10.1016/j.neubiorev.2019.03.015

Abstract

Fear is an emotion that serves as a driving factor in how organisms move through the world. In this review, we discuss the current understandings of the subjective experience of fear and the related biological processes involved in fear learning and memory. We first provide an overview of fear learning and memory in humans and animal models, encompassing the neurocircuitry and molecular mechanisms, the influence of genetic and environmental factors, and how fear learning paradigms have contributed to treatments for fear-related disorders, such as posttraumatic stress disorder. Current treatments as well as novel strategies, such as targeting the perisynaptic environment and use of virtual reality, are addressed. We review research on the subjective experience of fear and the role of autobiographical memory in fear-related disorders. We also discuss the gaps in our understanding of fear learning and memory, and the degree of consensus in the field. Lastly, the development of linguistic tools for assessments and treatment of fear learning and memory disorders is discussed.

Keywords: Autobiography; Fear; Linguistics; Neuroanatomy; Neuropharmacology; Subjective fear; Virtual reality.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Review

MeSH terms

Animals
Fear / physiology*
Humans
Learning / physiology*
Memory, Episodic*
Phobic Disorders* / physiopathology
Phobic Disorders* / therapy
Psycholinguistics*
Stress Disorders, Post-Traumatic* / physiopathology
Stress Disorders, Post-Traumatic* / therapy