József Haller. Neurobiological Bases of Abnormal Aggression and Violent Behaviour

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2 József Haller Neurobiological Bases of Abnormal Aggression and Violent Behaviour

3 Neurobiological Bases of Abnormal Aggression and Violent Behaviour

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5 József Haller Neurobiological Bases of Abnormal Aggression and Violent Behaviour

6 József Haller Department of Behavioral Neurobiology Institute of Experimental Medicine Budapest, Hungary ISBN ISBN (ebook) DOI / Springer Wien Heidelberg New York Dordrecht London Library of Congress Control Number: Springer-Verlag Wien 2014 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. Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher s location, in its current version, and permission for use must always be obtained from Springer. Permissions for use may be obtained through RightsLink at the Copyright Clearance Center. Violations are liable to prosecution under the respective Copyright Law. 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. While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed on acid-free paper Springer is part of Springer Science+Business Media (

7 Preface Understanding the brain control of aggression was greatly enhanced over the last decade. Out of the multitude of new developments, this book will primarily focus on two: the emergence of abnormal aggression models in animals and the introduction and expansion of brain imaging techniques in humans. Although apparently unrelated, these developments bridged an important gap between animal and human aggression research. In sharp contrast with human research where aggression-related psychopathologies are of major interest, animal research was for long dominated by laboratory models of natural aggressiveness. Newly developed models detached from this classical approach by mimicking etiological factors of aggression-related psychopathologies and by identifying deviant forms of aggression that arise as a consequence of these treatments. Thus, animal research gradually shifted from studying aggression as a natural phenomenon to studying models of abnormal aggression. Recently developed models made clear that laboratory equivalents of etiological factors induce profound changes in brain function and alter qualitatively the neural circuits that are activated by social conflict and that regulate aggressive behavior under these circumstances. Before the advent of brain imaging techniques, human research lacked adequate tools to study brain function. This is in sharp contrast with animal research where a wide range of advanced technologies were developed over the last decades. In lack of appropriate research tools, assumptions on human brain mechanisms were based on animal studies that were occasionally cross-checked by studies involving people with accidental brain lesions and by brain stimulation techniques that were rather infrequently employed. Brain imaging techniques provide powerful tools of investigation, which showed spectacular advancements over the last decade. New technologies not only allow the study of structural features but also reveal brain connectivity, neurotransmitter receptor profiles, and other important aspects of brain function. In brief, models of abnormal aggression made animal studies more relevant for human research, while brain imaging techniques made human research more relevant for understanding brain mechanisms. These newly acquired features of v

8 vi Preface the two main sides of aggression research have the potential to make them closer partners and to start a process of integration that is beneficial for both sides and for aggression research in general. The main aim of this book is to create a platform for interactive thinking. We strongly believe that the control of aggression in general and of abnormal aggressiveness in particular cannot be understood without integrating animal findings of translational value and human findings. Close interactions between the two sides offer human research the chance to take advantage of the depth of analysis allowed by the advanced neuroanatomical and neurofunctional methodologies currently used in animal research, while research on animal aggression will greatly benefit from incorporating information on the phenomenon it models. The two developments discussed here opened new channels of information exchange and created the possibility of jointly addressing the triple linkage of etiological factors, brain changes, and behavior and to unravel novel treatment opportunities that take into account all three. This book intends to be the first step towards the integration of concepts and findings that makes this possible. Budapest, Hungary József Haller

9 Contents 1 Normal and Abnormal Aggressions: Definitions and Operational Approaches Demarcating and Characterizing Aggression: Theoretical Definitions Basic Definitions Definitions for Subtypes Normal and Abnormal Aggressions: Basic Principles A Theoretical Classification of Aggressive Behaviors Quantifying Aggression: Operational Approaches Models of Normal Aggression in Animals Models of Abnormal Aggression in Animals Classification of Abnormal Aggression Models Normal and Abnormal Aggressions in Humans Classifications of Operational Approaches in Humans Definitions, Approaches, and the Validity of Conclusions Hormonal Determinants Hormones and Brain Function Testosterone Mechanisms of Action Developmental Effects on Aggression in Animals and Humans Postpubertal Effects in Animals: Normal and Abnormal Aggressions Does Testosterone Affect Aggression in Humans? Testosterone and Abnormal Aggression in Humans Overview Glucocorticoids Mechanisms of Action Normal Aggression in Animals Abnormal Aggression in Animals vii

10 viii Contents Healthy Human Controls Abnormal Aggression in Humans Overview Overall Evaluation of Hormonal Determinants Neural Circuits Subserving Aggression: General Models Animals Cats Rats Humans Outlook Focal Points of Aggression Control The Hypothalamus Hypothalamically Controlled Behaviors Hypothalamic Control of Aggression in Animals and Humans Hypothalamic Mechanisms of Abnormal Aggression in Animals The Human Case Overview: Etiological Factor-Dependent Alterations in the Hypothalamus The Prefrontal Cortex Prefrontal Anatomy of Violence: A Prelude An Overall Summary of the General View Problems with the General View The Psychological Landscape Hypothesis The Neural Network Hypothesis The Amygdala Structure and General Roles in Behavior Normal Aggression in Animals Abnormal Aggression in Animals Normal and Abnormal Aggressions in Humans Overview The Periaqueductal Gray The Role of the Periaqueductal Gray (PAG) in Behavioral Control The Role of the PAG in Animal Aggression The Role of the PAG in Human Aggression Overview The Role of Emerging Techniques in Understanding Aggression Optogenetics Epigenetics Functional Pharmacology Genetics and Pharmacogenetics Overview

11 Contents ix 6 Summary and Synthesis Who s Flying the Plane and What Kind of Plane? Behavior and Brain Function in Animal Aggression Normal Aggression Abnormal Aggression The Role of the Prefrontal Cortex Behavior and Brain Function in Human Aggression The Dual Theory of Aggression Types of Aggression and Brain Function Hormones Postscript References Index

12 Chapter 1 Normal and Abnormal Aggressions: Definitions and Operational Approaches The Latin original of the term aggression ( aggressio ) had a military connotation in ancient times and meant undertaking a task and assault. Its psychological and psychiatric meaning was acquired during the twentieth century; the definition hostile or destructive behavior was first recorded in 1912 in A. A. Brill s translation of Freud. 1 Hostile and destructive behavior, however, can be understood and measured in different ways especially when the term is used to denote behaviors expressed by different species. Understanding the neural control of a behavior necessitates the clear delimitation of the behavior that is controlled. While definitions on aggression are in no short supply, these often lack aspects that are crucial for this book: the cross-species validity of definitions, their corroboration with methods of measurement, and the clear delimitation of normal and abnormal forms. To address these issues, here we circumscribe aggressive behavior in two meanings, namely, in theoretical and practical terms. Firstly, we will review intensional definitions that specify the necessary and sufficient conditions to differentiate this behavior from others. This will be followed by extensional definitions that list its main forms and subcategories. While these theoretical constructs clearly demarcate aggressive behavior, they cannot be directly used in research because they do not provide means to measure it. These means are provided by more practical operational approaches, particularly by the methodologies that are employed in aggression research to quantify aggressiveness. Animal and human methodologies will be evaluated comparatively; the boundaries between normal and abnormal aggressions will be in focus throughout. The last section of this chapter examines the area of validity of conclusions that are based on particular operational approaches and their relevance for understanding aggression control. 1 J. Haller, Neurobiological Bases of Abnormal Aggression and Violent Behaviour, DOI / _1, Springer-Verlag Wien

13 2 1 Normal and Abnormal Aggressions: Definitions and Operational Approaches 1.1 Demarcating and Characterizing Aggression: Theoretical Definitions Basic Definitions In principle, there are two types of definitions for aggression : one focuses on external appearance (i.e., the form of behavior), while the other focuses on its functions. Behavioral form or phenomenological definitions highly preferred in the 1960s and 1970s are usually restrictive but have the advantage of being simple and easily applicable to both animals and humans. In plain terms, aggressiveness can be defined as a behavior that delivers noxious stimuli to another organism (Buss 1961) or somewhat more explicitly: any behavior directed towards the goal of harm and injury (Baron 1977; Zillman 1979). These clear-cut definitions immediately raise a simple but relevant question: why should one organism deliver noxious stimuli to another? The explanation is provided by the other type of basic definitions, which attribute functions to this behavior. Functional definitions are likely based on the common observation that aggressiveness is present in any species that is endowed with the capacity of performing it, from invertebrates to humans. 2 One cannot reasonably assume that aggressive behavior survived evolutionary pressures for hundreds of millions of years in so many species without providing some functional advantages. It is generally believed that aggression is the most efficient form of competition that bridges the gap between the limitedness of resources on one side and the individual needs of survival and the more general evolutionary need of leaving as many descendants as possible on the other side. Thus, the proximate function of aggression is resource competition that ensures survival, while the ultimate function is reproduction that ensures contribution to the gene pool of the next generation. This dual goal is achieved by fights over food, territory, mating partners, etc., and by protecting offspring by aggressive means. This utilitarian view on aggression was formulated very early (Darwin 1871) and was maintained ever since (see Archer 2009; Lindenfors and Tullberg 2011; Weiger and Bear 1988 as examples). Thus, individuals harm each other to get access to resources and to ensure gene transmission over generations in a world where resources are limited and the delivery of harm is more efficient than negotiation. 3 At the first sight, the functional definition applies to animals only, because survival and the ability to leave progeny rarely depend on aggression in humans. Human societies consist of highly interdependent individuals, which are expected to negotiate rather than fight for resources. Still, human aggression is often gain oriented; this type of human 2 For arthropods see Kravitz and Huber (2003); for lower animals see van Staaden et al. (2011) and Evans (1973). 3 Negotiation and sharing are viable options when resources are sufficient for all. This is not always the case.

14 1.1 Demarcating and Characterizing Aggression: Theoretical Definitions 3 behavior is commonly called instrumental aggression (Feshbach 1971). Moreover, particular forms of aggression (usually considered legitimate) serve survival in the form of self-defense, the defense of offspring, or the defense of others (Archer 2009; Björkqvist et al. 2000). Furthermore, intricate forms, e.g., relational and indirect aggressions, are means of social competition that are employed at a wide scale in human societies. Because human aggression may become a matter of survival and inclusive fitness under certain conditions, one should attribute functionality to human aggression as well. Taken together, these considerations show that (1) aggression is omnipresent in arthropods and vertebrates and is shown by all lower animals that are endowed with the capacity of performing it and (2) it confers competitive advantage in animals and has similar roles in people under particular conditions. A final clarification that intensional definitions need refers to the word harm. In his influential work on aggression, Lorez (1963) notes that crude forms of aggression (i.e., the delivery of injuries) gradually progress into symbolic actions that fulfill the function of communication. The reason is that aggressiveness involves considerable risks for both the recipient and perpetrator. Either of the fighting parties can suffer injuries, and both lose energy reserves that may become vital in a subsequent challenge (e.g., predator attack) (Haller 1995). Therefore, injurious behaviors not only are gradually replaced with but are also preceded by less risky behaviors, e.g., threat signals that offer the chance of withdrawal before the actual fight is started. Such forms of behavior are integrant parts of the aggressive repertoire of animals (see van Staaden et al for a review). Human aggression also entails threats, e.g., threatening facial expressions and body language, verbal warnings, etc. It is generally considered that threatening with physical harm is an aggressive act per se. On the other hand, harm should not always be understood in a physical sense. Manipulating social environments (e.g., by malicious gossiping, ignoring, and coercing) may hurt a person in a nondirect manner and may ultimately disrupt his/her social status (Bjorkqvist and Niemela 1992; Coccaro et al. 1997a, b; Galen and Underwood 1997; Gomes 2007; Paquette and Underwood 1999). Social manipulation is not uncommon in animals; the main behavioral tool is social exclusion in their case (see Sasaki and Uchida (2012) for a review and Goodall (1986) for studies in chimpanzees). Therefore, a more complete definition should make reference not only to harm and injury but also to threatening with these; in addition, it should consider harm in both physical and psychological terms (Björkqvist et al. 2000; Brower and Price 2001). Further specifications of the word harm include intentionality (to exclude accidental events) and exclude benefits for the victim (Berkowitz 1993, 1994; Björkqvist et al. 2000; Bushman and Anderson 2001; Feshbach 1971). As such, aggression includes neither accidental harm nor harm inflicted for positive ends (e.g., to discourage social parasites, to discipline offspring, or to maintain cooperative behavior; Clutton-Brock and Parker 1995). To avoid an impossibly complex sentence, we define aggression below by pointing out its essence and adding modifiers.

15 4 1 Normal and Abnormal Aggressions: Definitions and Operational Approaches Aggression is a behavioral means of resource competition that is based on the delivery of or threatening with harm. Harm should be understood in both physical and psychological terms, should be intentional, and should benefit the victim neither directly nor indirectly Definitions for Subtypes The definition adopted above shows that aggression is not a unitary phenomenon and cannot be the object of studies in such general terms. Therefore, aggression was divided into several subtypes along a variety of classification principles. The form of aggression is one such principle; in humans, subtypes are called physical, verbal, and indirect aggressions (Bjorkqvist and Niemela 1992; Gomes 2007; Paquette and Underwood 1999; Vaillancourt and Sunderani 2011). Physical aggression involves physical harm; verbal aggression (including body language) covers threats that aim at intimidating partners, while indirect aggression consists of social manipulation that inflicts psychological harm in most cases. In some papers, indirect aggression was restricted to or included aggression towards objects (Coccaro et al. 1997a, b; Crowe 1974). This approach was considered outdated by papers published later (Gomes 2007). We suggest here that aggression against objects (e.g., slamming doors) should be considered part of verbal aggression when its aim is intimidation and displaced aggression when it serves to channel off emotions. This issue will be detailed below. Rodent analogs of these behavioral categories include biting attacks (physical aggression), offensive threats (verbal aggression), and social exclusion (indirect aggression). Phenomenologically delimited subtypes can be graded according to their precise forms and the severity of consequences. For example, fighting with bare hands is considered milder than weapon use; injuring is a lesser form of aggression than killing (Björkqvist et al. 2000; Holm 1982). Similarly, body language and verbal threats may be perceived as graded versions of verbal aggression. Finally, indirect aggression can be divided into direct (conspicuous) and hidden forms (Gomes 2007). The reason and emotional background of aggression can also serve as criteria for typifying this behavior. Emotional and instrumental forms are the most widely used categories (Blair 2001; Feshbach 1971; Kempes et al. 2005; Lopez-Duran et al. 2009; Raine et al. 2006; van Bokhoven et al. 2005; van Honk et al. 2010). The former (often called reactive) consists of uncontrolled aggressive outbursts that are elicited by perceived threat or provocation. This type of aggression is characterized by high levels of bodily arousal. Instrumental aggression (also called proactive) is controlled and goal directed. It is usually associated with low levels of arousal. Emotional and instrumental aggressions are associated with different types of criminal aggression and aggression-related psychopathologies, as discussed below. There are several rodent models of abnormal aggression, where important aspects of emotional (reactive) and instrumental (proactive) aggression were mimicked (see below). A specific form of emotional responses is displaced