Cannabinoid Modulation of Emotion, Memory, and Motivation

Cannabinoid Modulation of Emotion, Memory, and Motivation

Patrizia Campolongo Liana Fattore Editors Cannabinoid Modulation of Emotion, Memory, and Motivation 1 3

Editors Patrizia Campolongo Dept. of Physiology and Pharmacology Sapienza University Rome Italy Liana Fattore Institute of Neuroscience CNR University of Cagliari Cagliari Italy ISBN 978-1-4939-2293-2 DOI 10.1007/978-1-4939-2294-9 ISBN 978-1-4939-2294-9 (ebook) Library of Congress Control Number: 2015930736 Springer New York Heidelberg Dordrecht London Springer Science+Business Media New York 2015 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com)

To Damiano, Matteo, Marco and Nicola, for their patience in conceding us to pursue our passion for science.

Preface Memory, emotions, reward, motivation, dependence, appetite, sociability. These are only some of the multiple domains in which the (endo)cannabinoid system is involved. We usually think of marijuana and cannabis derivatives as recreational compounds. But what do we know about their actions on the brain, about how the endocannabinoid system modulates such numerous and important aspects of our life? Are we really aware of the uniqueness of this, until recently unknown but, ubiquitous neuromodulatory system? What can we learn from recent progress in research? These are all questions that recent research allowed us to start addressing. After the finding of specific receptors that are activated by smoking marijuana, it was the time of the discovery of a number of endogenous marijuana-like substances called endocannabinoids followed by the identification of metabolic enzymes for such ligands. Other groundbreaking advances in the field then paved the way for an enthusiastic research activity on this fascinating regulatory system. And the more we know the more we want to know. This book is intended to offer an all-embracing overview of the most recent discoveries on the role played by the endocannabinoid system in the modulation of memory, emotions, reward and motivation, and how it interferes with the actions of other drugs of abuse and underlying neurotransmission systems. In Cannabinoid Modulation of Emotion, Memory, and Motivation leading experts in the field critically illustrate and discuss in dedicated chapters recent breakthroughs on the effects of cannabinoids on memory, learning and cognition, fearcoping strategies and emotional processing, motivation and reward. A particular emphasis is given to the delicate issues of cannabis use by adolescents and the emerging role of gender and sexual hormones in the frequency and consequences of its use, the problem of poly-substance abuse, and the diffusion of potent synthetic cannabinoids on the internet. The book is organized into three distinct sections. Part I focuses on the modulation of memory and emotions by cannabinoids, featuring the underlying neurobiology and emphasizing their effects on fear, anxiety and depression. Part II is centered on reward and motivation; it discusses subjective, cognitive, and social effects of cannabinoids and their impact of the motivational brain system with a particular vii

viii Preface attention on age and sex effects. Finally, interactions of cannabinoids with other drugs of abuse such as nicotine, alcohol, opioids and methamphetamine are illustrated in Part III, with a special focus on their interaction with the dopaminergic neurotransmission system. This book will stimulate curiosity toward research on (endo)cannabinoids from molecular neurobiology to behavior to therapeutic implications and will be of help to students, scientists and clinicians for better appreciating this captivating brain endogenous system and its powerful modulatory action. Patrizia Campolongo Liana Fattore

Contents Part I Cannabinoid Modulation of Memory and Emotions 1 Endocannabinoid Modulation of Memory for Emotionally Arousing Experiences... 3 Maria Morena and Patrizia Campolongo 2 Cannabinoids Modulation of Emotional and Non-Emotional Memory Processes After Stress... 23 Irit Akirav 3 The Hippocampal Endocannabinoid System in Different Memory Phases: Unveiling the CA1 Circuitry... 45 Jorge Alberto Quillfeldt and Lucas de Oliveira Alvares 4 Interactions Between Cannabinoid Signaling and Anxiety: A Comparative Analysis of Intervention Tools and Behavioral Effects... 73 Mano Aliczki and Jozsef Haller 5 Role of the Endocannabinoid System in Depression: from Preclinical to Clinical Evidence... 97 Vincenzo Micale, Katarina Tabiova, Jana Kucerova and Filippo Drago 6 Cannabinoid Control of Fear Responses... 131 Mathilde Metna-Laurent, Giovanni Marsicano and Edgar Soria-Gómez Part II Cannabinoid Modulation of Reward and Motivation 7 Subjective and Cognitive Effects of Cannabinoids in Marijuana Smokers... 159 Marie R. Ehrler, Erin C. McGlade and Deborah A. Yurgelun-Todd ix

x Contents 8 Endocannabinoid-Dopamine Interactions Shape Ethologically Relevant Behavior through Computation of Conditioned Stimuli... 183 Erik B. Oleson and Joseph F. Cheer 9 Synthetic Cannabinoid Effects on Behavior and Motivation... 205 William D. Wessinger, Jeffery H. Moran and Kathryn A. Seely 10 Cannabinoid Modulation of Rodent Ultrasonic Vocalizations in a Social Context: Communicative and Rewarding Properties... 225 Antonia Manduca, Louk J. M. J. Vanderschuren and Viviana Trezza 11 Age-Dependent Effects of Cannabinoids on Neurophysiological, Emotional, and Motivational States... 245 María-Paz Viveros and Eva María Marco 12 Gender Differences in Cannabis Addiction and Dependence... 283 Caroline Davis and Liana Fattore Part III Cannabinoid Interactions in Modulating Emotions and Reward 13 Cannabinoid-Nicotine Interactions... 329 Alessia Auber, Zuzana Justinova, Maria Scherma, Steven R. Goldberg and Leigh V. Panlilio 14 Cannabinoid-Alcohol Interactions... 363 Luis A. Natividad, Paola Maccioni, Loren H. Parsons and Giancarlo Colombo 15 Cannabinoid-Opioid Interactions... 393 Michael L. Miller, Benjamin Chadwick, Claudia V. Morris, Michael Michaelides and Yasmin L. Hurd 16 Interactions of Cannabis and Amphetamine-Type Stimulants... 409 Simone Tambaro and Marco Bortolato 17 Cannabinoid-Dopamine Interactions: Modulation of Midbrain DA Neurons by Endocannabinoids... 443 François Georges and Miriam Melis Erratum... E1

Contributors Irit Akirav Department of Psychology, University of Haifa, Haifa, Israel Mano Aliczki Department of Behavioural Neurobiology, Institute of Experimental Medicine, Budapest, Hungary Alessia Auber Preclinical Pharmacology Section, Behavioral Neuroscience Research Branch, Department of Health and Human Services, National Institute on Drug Abuse, IRP, Baltimore, MD, USA Marco Bortolato Department of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, Kansas, USA Patrizia Campolongo Department Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy Benjamin Chadwick Departments of Neuroscience and Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA Joseph F. Cheer University of Maryland School of Medicine, Baltimore, MD, USA Giancarlo Colombo Institute of Neuroscience-Cagliari, National Research Council (CNR), Monserrato, Italy Caroline Davis Department of Kinesiology and Health Sciences, York University, Toronto, Ontario, Canada Filippo Drago Department of Clinical and Molecular Biomedicine, Section of Pharmacology and Biochemistry, Medical School, University of Catania, Catania, Italy Marie R. Ehrler Department of Psychiatry, University of Utah School of Medicine, Salt Lake City, UT, USA xi

xii Contributors Liana Fattore Institute of Neuroscience-Cagliari, National Research Council (CNR), Monserrato, Italy CNR Institute of Neuroscience-Cagliari, National Research Council-Italy @ Department of Biomedical Sciences, University of Cagliari, Cittadella Universitaria di Monserrato, Monserrato, Cagliari, Italy François Georges IINS-UMR5297, CNRS, Bordeaux, France Steven R. Goldberg Preclinical Pharmacology Section, Behavioral Neuroscience Research Branch, Department of Health and Human Services, National Institute on Drug Abuse, IRP, Baltimore, MD, USA Jozsef Haller Department of Behavioural Neurobiology, Institute of Experimental Medicine, Budapest, Hungary Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary Yasmin L. Hurd Departments of Neuroscience and Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA Icahn School of Medicine at Mount Sinai, 1470 Madison Avenue, New York, NY, USA Zuzana Justinova Preclinical Pharmacology Section, Behavioral Neuroscience Research Branch, Department of Health and Human Services, National Institute on Drug Abuse, IRP, Baltimore, MD, USA Jana Kucerova Department of Pharmacology, CEITEC (Central European Institute of Technology) Masaryk University, Brno, Czech Republic Paola Maccioni Institute of Neuroscience-Cagliari, National Research Council (CNR), Monserrato, Italy Antonia Manduca Department of Science, Roma Tre University, Rome, Italy Eva María Marco Departamento de Fisiología (Fisiología Animal II), Facultad de Biología, Universidad Complutense de Madrid (UCM), Madrid, Spain Giovanni Marsicano University of Bordeaux, INSERM U862 NeuroCentre Magendie, Bordeaux, France Erin C. McGlade Department of Psychiatry, University of Utah School of Medicine, Salt Lake City, UT, USA Miriam Melis Department of Biomedical Sciences, University of Cagliari, Cagliari, Italy Mathilde Metna-Laurent University of Bordeaux, INSERM U862 NeuroCentre Magendie, Bordeaux, France

Contributors xiii Vincenzo Micale Department of Pharmacology, CEITEC (Central European Institute of Technology) Masaryk University, Brno, Czech Republic Michael Michaelides Departments of Neuroscience and Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA Michael L. Miller Departments of Neuroscience and Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA Jeffery H. Moran Arkansas Department of Health, Arkansas Public Health Laboratory, Little Rock, AR, USA Maria Morena Department Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy Claudia V. Morris Departments of Neuroscience and Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA Luis A. Natividad Research Associate, Committee on the Neurobiology of Addictive Disorders, The Scripps Research Institute, La Jolla, CA, USA Erik B. Oleson University of Maryland School of Medicine, Baltimore, MD, USA Lucas de Oliveira Alvares Psychobiology and Neurocomputing Lab - LPBNC Dept. of Biophysics, IB & Neurosciences Graduate Program, ICBS, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil Leigh V. Panlilio Preclinical Pharmacology Section, Behavioral Neuroscience Research Branch, Intramural Research Program, Department of Health and Human Services, National Institute on Drug Abuse, IRP, National Institutes of Health, Baltimore, MD, USA Loren H. Parsons Committee on the Neurobiology of Addictive Disorders, The Scripps Research Institute, La Jolla, CA, USA Jorge Alberto Quillfeldt Psychobiology and Neurocomputing Lab - LPBNC Dept. of Biophysics, IB & Neurosciences Graduate Program, ICBS, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil Maria Scherma Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, Cagliari, Italy Kathryn A. Seely Arkansas Department of Health, Arkansas Public Health Laboratory, Little Rock, AR, USA Edgar Soria-Gómez University of Bordeaux, INSERM U862 NeuroCentre Magendie, Bordeaux, France

xiv Contributors Katarina Tabiova Department of Pharmacology, CEITEC (Central European Institute of Technology) Masaryk University, Brno, Czech Republic Simone Tambaro Department of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, Kansas, USA Viviana Trezza Department of Science, Roma Tre University, Rome, Italy Louk J. M. J. Vanderschuren Department of Animals in Science and Society, Division of Behavioural Neuroscience, Utrecht University, Utrecht, The Netherlands María-Paz Viveros Departamento de Fisiología (Fisiología Animal II), Facultad de Biología, Universidad Complutense de Madrid (UCM), Madrid, Spain William D. Wessinger Department of Pharmacology and Toxicology, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, AR, USA Deborah A. Yurgelun-Todd Department of Psychiatry, University of Utah School of Medicine, Salt Lake City, UT, USA