The Psychobiology of Affective Development (PLE: Emotion)

Nathan A. Fox, Richard Davidson

• Publisher: Psychology Press
• Year: 2014
• ISBN:
  9781317596097
• Edition: 1
• Topic: Psychology
• Subtopic: Developmental Psychology
• Index: Psychology

Originally published in 1984, this was the first volume on this topic to appear in an emerging area of study at the time. The editors were selective in choosing their contributions to the volume to ensure that both the developmental and neuropsychological domains were well represented. One of the major goals was to foster greater contact and cross-fertilization between subdisciplines that they firmly believed should be more intimately connected. The result is this title, which can now be enjoyed in its historical context.

1	Neuroanatomical and Neurochemical Substrates of Affective Behavior

Ann E. Kelley

Louis Stinus

Universite de Bordeaux II
France

Is emotion a magic product, or is it a physiologic process which depends on an anatomic mechanism?

–J. W. Papez, 1937

INTRODUCTION

The study of affective or emotional behavior has evolved within several different disciplines. For example, ethologists, since Darwin’s early studies on the expression of emotion, have been primarily interested in the affective behavior of animals, and the various species-specific social interactions which such behavior entails. In developmental and social psychology, emphasis is placed on behavioral development and expression of affect in humans. Physiological psychology, on the other hand, has traditionally taken the approach of studying what cerebral structures mediate “emotions” and “feelings.” Even present-day psychiatry tends to view the psychopathology of affective behavior from separate perspectives: the psychodynamic, analytic school, and the approach of biological psychiatry, which considers the neural basis of psychiatric disorders.

Although these fields of study and investigation have developed along different lines, in recent years questions have been posed which necessitate more interdisciplinary approaches; for example, how can stages of neural development be correlated with development of behavior? Can the phenomenological profile of schizophrenia or mania be somehow reproduced in animals? Interest in neural substrates has expanded and has undoubtedly become relevant to a broader range of researchers. The aim of the present chapter is to present an overview of what is known about brain mechanisms and affective behavior, and it is particularly intended for those whose discipline is not strictly related to neuroscience.

The first part of the chapter reviews pioneering studies and theories of limbic system function. We then present more recent concepts, as well as provide basic anatomical figures to orient the reader. The last part of the chapter focuses on specific neurotransmitter pathways which appear to be involved in affective behavior and underscores the biochemical theories of mental illness. There are obviously clear limitations in such a wide-ranging endeavor, and it is not the scope of this paper to exhaustively review the literature or to present detailed neural mechanisms. However, we hope to construct a framework for speculation about the brain and affective behavior, and thus to provide a suitable “psychobiological perspective.”

NEUROANATOMICAL BASIS OF AFFECTIVE BEHAVIOR

The Limbic System in Historical Perspective

The term “limbic system,” which denotes a set of related neural structures and pathways in the brain, has its origin in the name “le grand lobe limbic” which was introduced by the French neurologist Paul Broca in 1878. Although Broca is best known for his description of the cerebral localization of language, his neuroanatomical observations led him to describe the limbic lobe, which consisted of the hippocampus and parahippocampal gyrus, structures which formed the underlying “limbus,” or border, of the cerebral cortical hemispheres. Somewhat later, anatomists such as Kölliker (1897), Gurdian (1925), and Herrick (1933), conducting the first comparative anatomical studies, described a group of cerebral structures which appeared to be closely linked to the olfactory system, such as hippocampus, olfactory lobe, septal region, and thus these structures were collectively named the “rhinencephalon” or olfactory brain. The amygdala, located deep within the temporal lobe, was also considered to be olfactory in function because of its close proximity to the nucleus of the olfactory tract. Anatomists of that day further recognized that rhinencephalic cortical structures were phylogenetically older (classified under such names as archipallium, paleopallium or allocortex), to be distinguished from newer cortical formations (isocortex or neocortex).

Although some early studies linked brain lesions with emotional disturbance (Bard, 1928; Fulton & Ingraham, 1929) and certainly the work of Cannon explored the physiological basis of emotion (1915, 1928), it was not until 1937 that the so-called rhinencephalon came to be associated with any function other than olfaction. Papez (1937), in a classical paper, proposed that a set of anatomically related structures which included the hypothalamus, anterior thalamic nuclei, cingulate gyrus, hippocampus, and their interconnections, mediated emotional expression and viscero-endocrine responses. This “proposed mechanism of emotion” was quite controversial at the time, as it challenged existing notions of the olfactory brain. However, it was becoming clear, at least from anatomical observations, that the term rhinencephalon was something of a misnomer (Brodal, 1947; Lang worthy, 1932); for example, it was noted that even in anosmatic mammals, such as the dolphin, the amygdala was highly developed (see Gloor, 1960; Richardson, 1973).

The Papez theory of emotion was developed and elaborated further by MacLean (1949), who introduced the concept of the limbic system. MacLean noted that the amygdala, hippocampus, basal forebrain regions such as septum, and specific cortical and thalamic areas all had close anatomical associations with the hypothalamus and postulated that these circuits modulated the affective, emotional quality of stimuli and were responsible for autonomic effector mechanisms. Further, he astutely remarked that the anatomical knowledge of these brain structures could provide important clues as to their function:

There are indications that the phylogenetically old brain (classically known as the rhinencephalon and arbitrarily referred to in this paper as the “visceral brain”) is largely concerned with visceral and emotional functions. This region of the brain appears to be so strategically situated as to be able to correlate every form of internal and external perception. In other words the possibility exists in this region for bringing into association not only oral (smell, taste, mouth) and visceral sensations, but also impressions from the sex organs, body wall, eye, and ear. And in contrast to the neopallium, the rhinencephalon has many strong connections with the hypothalamus for discharging its impressions, (p. 351)

Of further note is that MacLean suggested that understanding limbic functions had far-reaching implications for psychiatric and psychosomatic disorders.

About the same time, Klüver and Bucy (1939) carried out some remarkable experiments which were to have a fundamental influence on concepts about affect and the brain. They found that bilateral removal of the temporal lobe in monkeys resulted in striking changes in affective and social behavior. The lobectomized animals, formerly quite wild, became docile and tame and showed no fear reactions toward humans and other normally fear-provoking objects. They displayed no anger or willingness to fight when abused by other monkeys. Moreover, the monkeys showed indiscriminate dietary behavior, attempting to eat many inedible objects, and inappropriate or excessive sexuality. This abnormal behavior was characterized by a tendency to attend and react to every visual stimulus, termed “hypermetamorphosis” by the authors. They referred to the overall syndrome as “psychic blindness” because the monkeys appeared unable to perceive the meaning of stimuli. The psychic blindness did not result if only one lobe was removed or if bilateral lesions spared the temporal lobes. It is noteworthy that abnormal behavioral changes following temporal lobectomy were observed by Brown and Schäfer (1888) almost 50 years earlier, but their report went largely unnoticed.

Throughout the forties and fifties, a strong interest developed in the neuropsychological functions of cortical and subcortical “limbic” structures, and a considerable literature accrued about behavioral effects of brain lesions, both in animals and humans. Jacobsen (1935) noticed that chimpanzees deprived of their frontal cortex experienced learning deficits and showed changes in emotional reactivity. Subsequently the frontal and temporal cortices came to be associated with a wide variety of complex associative and sensory-affective functions (Harlow, Davis, Settlage, & Meyer, 1952; Hebb, 1939; Pribram & Bagshaw, 1953; Rosvold & Mishkin, 1950), and it was about this time that the notion and practice of psychosurgery was advanced (Moniz, 1936) when it became clear that emotional reactivity in humans was as drastically altered by certain cortical ablations as it was in animals.

Certain studies on the effects of lesions in subcortical limbic regions also supported the developing concept that a set of interconnected structures somehow modulated affective responses. For example, Wheatley (1944) found that lesions in the ventromedial hypothalamus in cats resulted in a “loss of favorable response to friendly treatment and a change to malevolence and savageness to a marked or extreme degree (p. 316)”. He noted that lesions outside this region did not produce the same effect. Brady and Nauta (1953) observed that surgical lesions in the septum resulted in significant increases in emotional reactivity of rats, or a syndrome known as “septal rage.”

Before discussing more recent views of the anatomy and function of the limbic system, it is worth mentioning some theoretical developments that significantly influenced research and thinking in this domain. The introduction into experimental psychology of the concepts of “drive” and “internal states,” elaborated by researchers studying animal learning and motivation (Hull, 1943; Mowrer, 1960; Richter, 1927; Seward, 1956; Sheffield & Campbell, 1954), had important consequences for the study of brain function, although such developments were quite separate at the time. The move away from the purely behaviorist view allowed speculation about how such factors as hunger, thirst, sexual drive, and hormonal states affected behavioral responses, and further, what physiological or neural systems mediated motivational states (see Bindra, 1968).

Yakovlev, in a theoretical article about “motility, behavior and the brain,” (1948) discussed relations between physiological and behavioral functions and neural correlates in a remarkably insightful manner. He states that all behavior can be divided into three spheres: (1) the sphere of visceral motility, such as cell metabolism, respiration, circulation, secretion, excretion; (2) the sphere of “motility of the outward expression of internal states” such as hunger, thirst, fear, rage, grief or pain, that is, the emotions (literally internal motions brought out); and (3) the sphere of motility of effectuation, which creates changes in the world around the animal, and in which the animal effects changes in the environment through the use of locomotion, and shapes and handles matter using his own body parts as tools (or, in the case of primates, creates tools). Yakovlev discussed the evolutionary significance of these concepts and drew parallels between the “behavioral spheres” and the development and organization of the nervous system: “Three central effector systems of gray matter and pathways gradually emerge in the wall of the neuraxial shift from within outward—the innermost, the intermediate, and the outermost system (p. 324).” The innermost zone, or endopallium, consisted of a core of gray matter of the brainstem, which was responsible for the regulatory and homeostatic mechanisms essential for life, the “visceral sphere” mentioned above. The intermediate zone, or mesopallium (common to all mammals), consisting of the limbic lobe and frontal lobe, was concerned with the emotive sphere. The ectopallium, or neocortex, was the outer and most phylogenetically new zone of the brain, consisting of both gray matter and immensely expanded white matter (neural pathways). This zone was important for the highest forms of cognition and behavior and in humans, symbolized thought, language, and achievement.

MacLean expanded these ideas, synthesizing principles of evolutionary theory, animal behavior, and comparative anatomy (1949, 1958, 1970). MacLean also emphasized in his writings the so-called three spheres of behavior and introduced the term “triune brain”: the ancient reptilian core, the old mammalian brain (limbic system), and new mammalian brain (See Fig. 1.1). Although present-day knowledge indicates that the three brains are a lot less distinct, anatomically and neurochemically, than MacLean pr...

Table of contents

• Cover
• Half Title
• Title Page
• Copyright Page
• Original Title Page
• Original Copyright Page
• Table of Contents
• Preface
• 1. Neuroanatomical and Neurochemical Substrates of Affective Behavior
• 2. Cerebral Asymmetry and Behavioral Laterality: Some Psychobiological Considerations
• 3. The Development of Affect in Rhesus Monkeys
• 4. The Ontogenesis of Human Social Signals: From Biological Imperative to Symbol Utilization
• 5. Facial Communication of Emotion in Early Infancy
• 6. Infant Crying and the Development of Communication
• 7. Lateralization of Emotion: A Model and the Evidence
• 8. Asymmetries in Affective Facial Expression: Behavior and Anatomy
• 9. The Development of Functional Brain Asymmetry in the Regulation of Emotion
• 10. Hemispheric Substrates of Affect: A Developmental Model
• Author Index
• Subject Index