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Current Understanding of Fear Learning and Memory in Humans And 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 Haas, Stefan Hofmann, Maria Kangas, Elizabeth Kensinger, Christopher Lowry, Hilary Marusak, et al. To cite this version: Jacob Raber, Shahar Arzy, Julie Boulanger Bertolus, Brendan Depue, Haley Haas, et al.. 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. Neuroscience & Biobehavioral Reviews, Oxford: Elsevier Ltd., 2019, 105, pp.136-177. 10.1016/j.neubiorev.2019.03.015. hal-02284719 HAL Id: hal-02284719 https://hal.archives-ouvertes.fr/hal-02284719 Submitted on 9 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Neuroscience and Biobehavioral Reviews 105 (2019) 136–177 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review article Current understanding of fear learning and memory in humans and animal T models and the value of a linguistic approach for analyzing fear learning and memory in humans ⁎ Jacob Rabera,b, , Shahar Arzyc, Julie Boulanger Bertolusd, Brendan Depuee, Haley E. Haasf, Stefan G. Hofmanns, Maria Kangasg, Elizabeth Kensingerh, Christopher A. Lowryi, Hilary A. Marusakj, Jessica Minnierk, Anne-Marie Moulyd, Andreas Mühlbergerl,m, Seth Davin Norrholmf, Kirsi Peltonenn, Graziano Pinnao, Christine Rabinakj, Youssef Shibanl,m, Hermona Soreqp, Michael A. van der Kooijq, Leroy Lower, Leah T. Weingastf, Paula Yamashitak, Sydney Weber Boutrosa a Department of Behavioral Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA b Departments of Neurology and Radiation Medicine, and Division of Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA c Department of Medical Neurobiology, Hebrew University, Jerusalem 91904, Israel d Lyon Neuroscience Research Center, CNRS-UMR 5292, INSERM U1028, Université Lyon, Lyon, France e Departments of Psychological and Brain Sciences and Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, USA f Department of Psychiatry and Behavioral Science, Emory University School of Medicine, Atlanta, GA, USA g Department of Psychology, Macquarie University, Sydney, Australia h Department of Psychology, Boston College, Boston, MA, USA i Department of Integrative Physiology and Center for Neuroscience, University of Colorado Boulder, Boulder, CO, USA j Department of Pharmacy Practice, Wayne State University, Detroit, MI, USA k School of Public Health, Oregon Health & Science University, Portland, OR, USA l Department of Psychology (Clinical Psychology and Psychotherapy), University of Regensburg, Regensburg, Germany m PFH – Private University of Applied Sciences, Department of Psychology (Clinical Psychology and Psychotherapy Research), Göttingen, Germany n Faculty of Social Sciences/Psychology, Tampere University, Tampere, Finland o The Psychiatric Institute, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA p Department of Biological Chemistry, Edmond and Lily Safra Center of Brain Science and The Institute of Life Sciences, Hebrew University, Jerusalem 91904, Israel q Translational Psychiatry, Department of Psychiatry and Psychotherapy, Universitatsmedizin der Johannes Guttenberg University Medical Center, Mainz, Germany r Neuroqualia, Nova Scotia, Canada s Department of Psychological and Brain Sciences, Boston University, Boston, MA, USA Abbreviations: ACC, anterior cingulate cortex; AChE, acetylcholinesterase; AET, autobiographic episodic training; AMPAR, AMPA receptor; AMT, Autobiographical Memory Test; apoE, apolipoprotein E; apoE2, E2; apoE3, E3; apoE4, E4; BDNF, brain-derived neurotrophic factor; CAPS, Clinician Administered PTSD Scale; CAVE, computer automatic virtual environment; CB1, type 1 cannabinoid receptors; CBD, cannabidiol; CBM, Cognitive Bias Modification; COMET, Competitive Memory Training; CR, conditioned fear response; CRH, corticotropin-releasing hormone; CS, conditioned stimulus; CSF, cerebrospinal fluid; DCS, D-cycloserine; DLPFC, dorsal lateral prefrontal cortex; DMN, default mode network; fMRI, functional magnetic resonance imaging; HMD, head mounted display; HPA, hypothalamic- pituitary-adrenal; Ig, immunoglobulin; l, long; LC, locus coeruleus; LPFC, lateral prefrontal cortex; LTP, long-term potentiation; MDD, major depressive disorder; MEST, Memory Specificity Training; miR, microRNA; miRNA, microRNAs; MPFC, medial prefrontal cortex; NE, norepinephrine; NMDA, N-methyl-D-aspartate; OCD, obsessive compulsive disorder; OFC, orbital frontal cortex; OGM, overgeneral autobiographical memory; PAS, pregnanolone sulfate; PE, Prolonged Exposure Therapy; PEA, palmitoylethanolamide; PFC, prefrontal cortex; PPAR, peroxisome proliferator-activated receptor; PSA, polysialylation; PTSD, posttraumatic stress disorder; s, short; SBSS, selective brain steroidogenic stimulant; SCEPT, Sentence Completion for Events of the Past Test; SNP, single nucleotide polymorphism; SSRI, selective serotonin reuptake inhibitor; TEMPau, Test Episodique de Memoire du Passe autobiographique; THC, Δ9-tetrahydrocannibinol; TSPO, translocator protein; US, unconditioned stimulus; VLPFC, ventral lateral prefrontal cortex; VMPFC, ventral medial prefrontal cortex; VR, virtual reality; VRET, Virtual Reality Exposure Therapy ⁎ Corresponding author at: Departs of Behavioral Neuroscience, Neurology, and Radiation Medicine, and Division of Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR, USA. E-mail address: [email protected] (J. Raber). https://doi.org/10.1016/j.neubiorev.2019.03.015 Received 24 August 2018; Received in revised form 30 January 2019; Accepted 18 March 2019 Available online 07 April 2019 0149-7634/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). J. Raber, et al. Neuroscience and Biobehavioral Reviews 105 (2019) 136–177 ARTICLE INFO ABSTRACT Keywords: Fear is an emotion that serves as a driving factor in how organisms move through the world. In this review, we Fear discuss the current understandings of the subjective experience of fear and the related biological processes Virtual reality involved in fear learning and memory. We first provide an overview of fear learning and memory in humans and Linguistics animal models, encompassing the neurocircuitry and molecular mechanisms, the influence of genetic and en- Autobiography vironmental factors, and how fear learning paradigms have contributed to treatments for fear-related disorders, Subjective fear such as posttraumatic stress disorder. Current treatments as well as novel strategies, such as targeting the Neuroanatomy Neuropharmacology perisynaptic environment and use of virtual reality, are addressed. We review research on the subjective ex- perience 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 develop- ment of linguistic tools for assessments and treatment of fear learning and memory disorders is discussed. 1. Background/introduction 1.1. Definition of fear This review is being undertaken as part of the ‘The Human Fear is defined as “a: an unpleasant often strong emotion caused by Affectome Project’, an initiative organized in 2016 by a non-profit or- anticipation or awareness of danger; b (1): an instance of this emotion; ganization called Neuroqualia. To launch the Human Affectome (2): a state marked by this emotion” (Merriam-Webster, 2017). In line Project, a workshop was organized in Halifax, Nova Scotia, on August 4 with recent arguments by LeDoux and Hofmann (2018), here we re- and 5, 2016. The project aims to produce a series of overarching re- strict the use of the term ‘emotion’ to subjective experiences. In their views that can summarize much of what is currently known about af- recent review, LeDoux and Hofmann refer to this view of fear as a fective neuroscience while simultaneously exploring the language that subjective emotional experience as the neuro-cognitive approach, in we use to convey feelings and emotions. The goal of this project was to which subjective fear emerges from higher-order processing. This view address two related issues: (1) to develop a comprehensive and robust in turn is based on arguments that emotional experiences are “cognitive functional model for emotions and feelings that can serve as a common constructions based on conceptualizations of situations (Barrett, 2006, focal point for research in the field and to avoid inconsistent constructs 2017; Barrett and Russell, 2015) or higher-order states that emerge as a (Izard, 2007); and (2) to support the neurophysiological and anatomical result of the
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