Decision Neuroscience

An Integrative Perspective

Jean-Claude Dreher, Léon Tremblay

• Publisher: Academic Press
• Year: 2016
• ISBN:
  9780128053317
• Topic: Medicine
• Subtopic: Physiology

Decision Neuroscience addresses fundamental questions about how the brain makes perceptual, value-based, and more complex decisions in non-social and social contexts. This book presents compelling neuroimaging, electrophysiological, lesional, and neurocomputational models in combination with hormonal and genetic approaches, which have led to a clearer understanding of the neural mechanisms behind how the brain makes decisions. The five parts of the book address distinct but inter-related topics and are designed to serve both as classroom introductions to major subareas in decision neuroscience and as advanced syntheses of all that has been accomplished in the last decade.

Part I is devoted to anatomical, neurophysiological, pharmacological, and optogenetics animal studies on reinforcement-guided decision making, such as the representation of instructions, expectations, and outcomes; the updating of action values; and the evaluation process guiding choices between prospective rewards. Part II covers the topic of the neural representations of motivation, perceptual decision making, and value-based decision making in humans, combining neurcomputational models and brain imaging studies. Part III focuses on the rapidly developing field of social decision neuroscience, integrating recent mechanistic understanding of social decisions in both non-human primates and humans. Part IV covers clinical aspects involving disorders of decision making that link together basic research areas including systems, cognitive, and clinical neuroscience; this part examines dysfunctions of decision making in neurological and psychiatric disorders, such as Parkinson's disease, schizophrenia, behavioral addictions, and focal brain lesions. Part V focuses on the roles of various hormones (cortisol, oxytocin, ghrelin/leptine) and genes that underlie inter-individual differences observed with stress, food choices, and social decision-making processes. The volume is essential reading for anyone interested in decision making neuroscience.

With contributions that are forward-looking assessments of the current and future issues faced by researchers, Decision Neuroscience is essential reading for anyone interested in decision-making neuroscience.

• Provides comprehensive coverage of approaches to studying individual and social decision neuroscience, including primate neurophysiology, brain imaging in healthy humans and in various disorders, and genetic and hormonal influences on decision making
• Covers multiple levels of analysis, from molecular mechanisms to neural-systems dynamics and computational models of how we make choices
• Discusses clinical implications of process dysfunctions, including schizophrenia, Parkinson's disease, eating disorders, drug addiction, and pathological gambling
• Features chapters from top international researchers in the field and full-color presentation throughout with numerous illustrations to highlight key concepts

Part I

Animal Studies on Rewards, Punishments, and Decision-Making

Outline

Chapter 1. Anatomy and Connectivity of the Reward Circuit

Chapter 2. Electrophysiological Correlates of Reward Processing in Dopamine Neurons

Chapter 3. Appetitive and Aversive Systems in the Amygdala

Chapter 4. Ventral Striatopallidal Pathways Involved in Appetitive and Aversive Motivational Processes

Chapter 5. Reward and Decision Encoding in Basal Ganglia: Insights From Optogenetics and Viral Tracing Studies in Rodents

Chapter 6. The Learning and Motivational Processes Controlling Goal-Directed Action and Their Neural Bases

Chapter 7. Impulsivity, Risky Choice, and Impulse Control Disorders: Animal Models

Chapter 8. Prefrontal Cortex in Decision-Making: The Perception—Action Cycle

Chapter 1

Anatomy and Connectivity of the Reward Circuit

S.N. Haber University of Rochester School of Medicine, Rochester, NY, United States

Abstract

While cells in many brain regions are responsive to reward, the cortical–basal ganglia circuit is at the heart of the reward system. The key structures in this network are the anterior cingulate cortex, the orbital prefrontal cortex, the ventral striatum, the ventral pallidum, and the midbrain dopamine neurons. In addition, other structures, including the dorsal prefrontal cortex, amygdala, thalamus, and lateral habenular nucleus, are key components in regulating the reward circuit. Connectivity between these areas forms a complex neural network that is topographically organized, thus maintaining functional continuity through the corticobasal ganglia pathway. However, the reward circuit does not work in isolation. The network also contains specific regions in which convergent pathways provide an anatomical substrate for integration across functional domains.

Keywords

Cognitive control; Cortical–basal ganglia network; Dopamine; Integrative circuits; Prefrontal cortex; Reward circuit

Introduction

The reward circuit is a complex neural network that underlies the ability to effectively assess the likely outcomes of different choices. A key component to good decision-making and appropriate goal-directed behaviors is the ability to accurately evaluate reward value, predictability, and risk. While the hypothalamus is central for processing information about basic, or primary, rewards higher cortical and subcortical forebrain structures are engaged when complex choices about these fundamental needs are required. Moreover, choices often involve secondary rewards, such as money, power, challenge, etc., that are more abstract (compared to primary needs), and not as dependent on direct sensory stimulation. Although cells that respond to various aspects of reward such as anticipation, value, etc., are found throughout the brain, at the center of this neural network is the ventral corticobasal ganglia circuit. The basal ganglia (BG) are traditionally considered to process information in parallel and segregated functional streams consisting of reward processing, cognition, and motor control areas [1]. Moreover, within the ventral BG, there are microcircuits thought to be associated with various aspects of reward processing. However, a key component for learning and adaptation of goal-directed behaviors is the ability not only to evaluate various aspects of reward but also develop appropriate action plans and inhibit maladaptive choices on the basis of previous experience. This requires integration between various aspects of reward processing as well as interaction between reward circuits and brain regions involved in cognition. Thus, while parallel processing provides throughput channels by which specific actions can be expressed while others are inhibited, the BG also plays a central role in learning new procedures and associations, implying the necessity for integrative processing across circuits. Indeed, we now know that the network contains multiple regions in which integration across circuits occurs [2–8]. Therefore, while the ventral BG network is at the heart of reward processing, it does not work in isolation. This chapter addresses not only the connectivities within this circuit, but also how this circuit anatomically interfaces with other BG circuits. Reward and aversive processes work together in learning and decision-making. Aversive processing associated with punishment and negative outcomes is addressed by other authors in this book.

The frontal–BG network, in general, mediates all aspects of action planning, including reward and motivation, cognition, and motor control. However, specific regions within this network play a unique role in various aspects of reward processing and evaluation of outcomes, including reward value, anticipation, predictability, and risk. The key structures are prefrontal areas [anterior cingulate cortex (ACC) and orbital prefrontal cortex (OFC)], the ventral striatum (VS), the ventral pallidum (VP), and the midbrain dopamine (DA) neurons. The ACC and OFC prefrontal areas mediate different aspects of reward-based behaviors, error prediction, value, and the choice between short- and long-term gains. Cells in the VS and VP respond to anticipation of reward and reward detection (see Chapter 4). Reward-prediction and error-detection signals are generated, in part, from the midbrain DA cells (see Schultz in this volume). While the VS and the ventral tegmental area (VTA) DA neurons are the BG areas most commonly associated with reward, reward-responsive activation is not restricted to these, but found throughout the striatum and substantia nigra pars compacta (SNc). In addition, other structures including the dorsal prefrontal cortex (DPFC), amygdala, hippocampus, thalamus, subthalamic nucleus (STN), and lateral habenula (LHb) are part of the reward circuit (Fig. 1.1).

Figure 1.1 Schematic illustrating key structures and pathways of the reward circuit. Shaded areas and gray arrows represent the basic ventral cortical–basal ganglia structures and connections. Amy, amygdala; dACC, dorsal anterior cingulate cortex; DPFC, dorsal prefrontal cortex; DS, dorsal striatum; Hipp, hippocampus; Hypo, hypothalamus; LHb, lateral habenula; MD, mediodorsal nucleus of the thalamus; OFC, orbital frontal cortex; PPT, pedunculopontine nucleus; SN, substantia nigra pars compacta; STN, subthalamic nucleus; THAL, thalamus; vmPFC, ventral medial prefrontal cortex; VP, ventral pallidum; VS, ventral striatum; VTA, ventral tegmental area.

Prefrontal Cortex

Although cells throughout the cortex fire in response to various aspects of reward processing, the main components of evaluating reward value and outcome are the orbital (OFC) and anterior cingulate (ACC) prefrontal cortices. These regions comprise several specific cortical areas: the orbital cortex is divided into areas 11, 12, 13, 14, and, often, caudal regions referred to as either parts of the insular cortex or periallo- and proisocortical areas; the ACC is divided into dorsal and subgenual regions, areas 24, 25, and 32 [9,10]. Based on specific roles for mediating different aspects of reward processing and emotional regulation, these regions can be functionally grouped into: (1) the OFC; (2) the ventral medial prefrontal cortex (VMPFC), which includes medial OFC and subgenual ACC; and (3) the dorsal ACC (DACC). In addition to the DACC, OFC, and VMPFC, the DPFC, in particular, areas 9 and 46, are engaged when working memory is required for monitoring incentive-based behavioral responses. The DPFC also encodes reward amount and becomes active when anticipated rewards signal future outcomes [11,12].

A key function of the OFC is to link sensory representations of stimuli to outcomes, which is consistent with its connections to both sensory and reward-related regions [12–15]. The OFC can be generally parceled into somewhat functionally different regions based on a caudal–rostral axis, with more caudal regions receiving stronger inputs from primary sensory areas and rostral regions connected to highly processed sensory areas. The OFC's unique access to both primary and highly processed sensory information, coupled with connections to the amygdala and cingulate, explains many of the functional properties of the region. Indeed, the two cardinal tests of OFC function are reward devaluation paradigms and stimulus-outcome reversal learning [16–18], both of which have been demonstrated with OFC lesions across species. Consistent with connectional differences between caudal and rostral OFC, there is an apparent gradient between primary reward representations in more caudal OFC/insular cortex and representations of secondary rewards such as money in more rostral OFC regions [19]. Such dissociations may rely on the differential inputs from early versus higher sensory representations to caudal versus rostral and OFC, respectively, or amygdala connections to caudal OFC and dorsolateral prefrontal cortex and a frontal pole to rostral OFC.

In contrast to the OFC, the ACC has a relative absence of sensory connections, but contains within in it a representation of many diverse frontal lobe functions, including motivation cognition and motor control, which is reflected in its widespread connections with other limbic, cognitive, and motor cortical areas. This is a complex area, but the overall role of the ACC appears to be involved in monitoring these functions for action selection [20–22]. Overall, the ACC can be divided functionally along its dorsal–ventral axis. The ventral ACC (areas 25 and ventral parts of 32) is closely associated with visceral and emotional functions and has strong connections to the hypothalamus, amygdala, and hippocampus. From a functional perspective, imaging and lesion studies have identified an area referred to as the VMPFC. Depending on the specific study, this region may include different combinations of these regions, but overall involves area 25, parts of 32, medial OFC (area 14 and 11), and ventromedial area 10. VMPFC cells track valu...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• List of Contributors
• Preface
• Part I. Animal Studies on Rewards, Punishments, and Decision-Making
• Part II. Human Studies on Motivation, Perceptual, and Value-Based Decision-Making
• Part III. Social Decision Neuroscience
• Part IV. Human Clinical Studies Involving Dysfunctions of Reward and Decision-Making Processes
• Part V. Genetic and Hormonal Influences on Motivation and Social Behavior
• Index