Cannabinoid Modulation of Emotion, Memory, and Motivation

Patrizia Campolongo • Liana FattoreEditors

Cannabinoid Modulation of Emotion, Memory, and Motivation

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ISBN 978-1-4939-2293-2 ISBN 978-1-4939-2294-9 (eBook)DOI 10.1007/978-1-4939-2294-9

Library of Congress Control Number: 2015930736

Springer New York Heidelberg Dordrecht London© Springer Science+Business Media New York 2015This 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.

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EditorsPatrizia CampolongoDept. of Physiology and PharmacologySapienza UniversityRomeItaly

Liana FattoreInstitute of Neuroscience CNRUniversity of CagliariCagliariItaly

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

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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 en-thusiastic 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 ex-perts in the field critically illustrate and discuss in dedicated chapters recent break-throughs on the effects of cannabinoids on memory, learning and cognition, fear-coping 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 modula-tion of memory and emotions by cannabinoids, featuring the underlying neurobiol-ogy 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

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attention on age and sex effects. Finally, interactions of cannabinoids with other drugs of abuse such as nicotine, alcohol, opioids and methamphetamine are illus-trated 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 CampolongoLiana Fattore

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Contents

Part I Cannabinoid Modulation of Memory and Emotions

1 Endocannabinoid Modulation of Memory for Emotionally Arousing Experiences .............................................................................. 3Maria Morena and Patrizia Campolongo

2 Cannabinoids Modulation of Emotional and Non-Emotional Memory Processes After Stress ............................................................... 23Irit Akirav

3 The Hippocampal Endocannabinoid System in Different Memory Phases: Unveiling the CA1 Circuitry ...................................... 45Jorge Alberto Quillfeldt and Lucas de Oliveira Alvares

4 Interactions Between Cannabinoid Signaling and Anxiety: A Comparative Analysis of Intervention Tools and Behavioral Effects .... 73Mano Aliczki and Jozsef Haller

5 Role of the Endocannabinoid System in Depression: from Preclinical to Clinical Evidence .............................................................. 97Vincenzo Micale, Katarina Tabiova, Jana Kucerova and Filippo Drago

6 Cannabinoid Control of Fear Responses ............................................... 131Mathilde 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 ............................................................................. 159Marie R. Ehrler, Erin C. McGlade and Deborah A. Yurgelun-Todd

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8 Endocannabinoid-Dopamine Interactions Shape Ethologically Relevant Behavior through Computation of Conditioned Stimuli ............................................................................. 183Erik B. Oleson and Joseph F. Cheer

9 Synthetic Cannabinoid Effects on Behavior and Motivation .............. 205William D. Wessinger, Jeffery H. Moran and Kathryn A. Seely

10 Cannabinoid Modulation of Rodent Ultrasonic Vocalizations in a Social Context: Communicative and Rewarding Properties ........ 225Antonia Manduca, Louk J. M. J. Vanderschuren and Viviana Trezza

11 Age-Dependent Effects of Cannabinoids on Neurophysiological, Emotional, and Motivational States ..................... 245María-Paz Viveros and Eva María Marco

12 Gender Differences in Cannabis Addiction and Dependence .............. 283Caroline Davis and Liana Fattore

Part III Cannabinoid Interactions in Modulating Emotions and Reward

13 Cannabinoid-Nicotine Interactions ........................................................ 329Alessia Auber, Zuzana Justinova, Maria Scherma, Steven R. Goldberg and Leigh V. Panlilio

14 Cannabinoid-Alcohol Interactions ......................................................... 363Luis A. Natividad, Paola Maccioni, Loren H. Parsons and Giancarlo Colombo

15 Cannabinoid-Opioid Interactions........................................................... 393Michael L. Miller, Benjamin Chadwick, Claudia V. Morris, Michael Michaelides and Yasmin L. Hurd

16 Interactions of Cannabis and Amphetamine-Type Stimulants ............ 409Simone Tambaro and Marco Bortolato

17 Cannabinoid-Dopamine Interactions: Modulation of Midbrain DA Neurons by Endocannabinoids ................................... 443François Georges and Miriam Melis

Erratum .......................................................................................................... E1

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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

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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

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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