Anatomy of Neuropsychiatry

The New Anatomy of the Basal Forebrain and Its Implications for Neuropsychiatric Illness

Lennart Heimer, Gary W. Van Hoesen, Michael Trimble, Daniel S. Zahm

• Publisher: Academic Press
• Year: 2007
• Print ISBN: 9780123742391
• eBook ISBN: 9780080555126
• Topic: Psychology
• Subtopic: Clinical Psychology
• Index: Psychology

Anatomy of Neuropsychiatrypresents the anatomical systems that take part in the scientific and clinical study of emotional functions and neuropsychiatric disorders. It discusses the limbic system—the cortical and subcortical structures in the human brain involved in emotion, motivation, and emotional association with memory—at length and how this is no longer a useful guide to the study of psychiatric disorders. The book provides an understanding of brain anatomy, with an emphasis on the new anatomical framework which has emerged during the last quarter century. The goal is to help the reader develop an understanding of the gross anatomical organization of the human forebrain.- A re-evaluation of brain anatomy, with an emphasis on the new anatomical framework which has emerged during the last quarter century- A compellingly expanded conceptualization of Broca's famous limbic lobe- Clinical and basic science boxes highlighting specific concepts, structures, or neuronal circuits from a clinical perspective

1

THE LIMBIC SYSTEM; A CONCEPT IN PERPETUAL SEARCH FOR A DEFINITION

Publisher Summary

This chapter discusses the concept, birth, and continuous evolution of the limbic system. The concept is based on Paul MacLean’s studies of temporal lobe epilepsy and James Papez’s highly speculative theory of a central mechanism of emotion. The concept is supported with evidence from the clinical literature on the symptoms following lesions of various parts of the “Papez circuit.” Further elaboration of the concept involves the subdivision of the limbic system into three nuclear groups: amygdala, septum, and anterior thalamic nuclear complex. These nuclear groups are considered the hubs for neuronal communication between the limbic cortex and the brainstem. The non-inclusion of the cerebellum as an integral part of the limbic system is analyzed. There is no end in sight regarding the evolution of the limbic system. The problem with the concept of the limbic system as an emotional mechanism is traced back to the attribution of emotional functions to a number of closely related anatomical structures with close relation to the hypothalamus (including the mammillary body) with hardly any experimental evidence that any of them, except the hypothalamus, is related to emotional functions.

Chapter Outline

1.1. The Birth of the Limbic System

1.2. The Continuing Evolution of the Limbic System

1.2.1. The “Limbic Midbrain Area” of Nauta

1.2.2. “The Greater Limbic System” of Nieuwenhuys

1.3. Why Isn’t the Cerebellum an Integral Part of the Limbic System?

1.4. The Evolution of the Limbic System: No End in Sight

1.1 THE BIRTH OF THE LIMBIC SYSTEM

The concept of the limbic system was proposed by Paul MacLean (1949; 1952) based on his own studies of temporal lobe epilepsy and James Papez’s proposal that “the hypothalamus, the anterior thalamic nuclei, the gyrus cinguli, the hippocampus and their interconnections constitute a harmonious mechanism which may elaborate the functions of central emotion, as well as participate in emotional expression” (Papez, 1937). Papez’s highly speculative theory of a central mechanism of emotion was based on studies by Cannon (1929), Bard (1928), and others, who promoted a central origin of emotion with the hypothalamus as a key structure in the expression of emotions (see Clinical Box 1). Papez supported his theory with evidence from the clinical literature on the symptoms following lesions of various parts of his circuit (known widely as the “Papez circuit”; Fig. 1.1). The inclusion of the hippocampus, for instance, was supported by the observation that Negri bodies, which are part of the pathology of rabies (characterized by intense emotional symptoms), are present in hippocampal pyramidal cells. Papez also found evidence in the clinical literature that the cingulate gyrus is “the seat of dynamic vigilance by which environmental experiences are endowed with an emotional consciousness” (Papez, 1937).

CLINICAL BOX 1 History of the Limbic System

The historical importance of the limbic system concept, ill-defined and confused as it is, should not be underestimated. It has been known for centuries that people suffer from what may loosely be referred to as emotional disorders, with many suggested potential causes that differ, depending on the historical epoch that is chosen. Most famous and relevant to this discussion is a statement by the Greek philosopher-physician Hippocrates that “from the brain come joys, delights, laughter and sports, and sorrows, griefs, despondency and lamentations…. and by the same organ we become mad and delirious, and terrors and fears assail us” (Adams, 1939). At the time of Hippocrates’ writing, many disorders, from epilepsy to madness, were thought to be the result of divine influence. Hippocrates opined that they are essentially somatic in origin and that the right approach to understanding them is through the natural sciences.

Although great strides in neuroanatomy and neurophysiology were made in the 19th century, there was little progress in understanding how emotions are represented neurologically. At the end of the century, William James suggested that the emotions are derived from peripheral sensory inputs to the brain, which activate motor outputs—and the resulting bodily sensations are perceived as emotion (James, 1884). As discussed in the book The Emotions (James and Lange, 1922), the Danish scientist C. G. Lange stated a similar hypothesis in 1885; therefore, the theory is often referred to as the James-Lange theory. In a nutshell, we do not run away from something because we are frightened, but we experience fear because we are running away. However, there was no obvious cerebral location for the generation of the emotions, although the sensory experiences were known to be received in the parietal cortex. The James-Lange hypothesis was soon tested and appeared to be wrong on two counts. First, it was demonstrated in animals that removal of the cerebral cortex on both sides did not abolish the expression of emotion (Vanderwolf et al., 1978; Whishaw, 1990). Further, it was revealed that stimulation of various structures buried deep within the brain could lead to the release of emotion. These observations formed the basis for a neuroscience revolution. That certain brain structures could form the foundation of an emotional brain system was a stunning conceptual departure for neurology and became a launch pad for the discipline of behavioral neurology—that is, that branch of neurology that tries to understand how the brain modulates and relates to behavior and neuropsychiatry.

Apropos is the Jamesian or “bodily feedback” theory, it may yet contain a kernel of truth (Damasio, 1996; LeDoux, 1996). Sensory stimuli from various body parts involved in emotional expressions are no doubt closely integrated with brain structures and circuits involved in emotional functions. In fact, it may not be too far-fetched to paraphrase Lautin (2001): “Peripheral (James) and central (Papez-MacLean) theories of emotions are two sides of the same coin.” One of the criticisms of MacLean’s limbic system concept or central theory of emotion was that the key structures involved seemed relatively isolated from the isocortex. It was as if the rider (the neocortical mantle) lacked reins with which to control the horse (the limbic system). This seemed to imply some self-contained arrangement, and if there was a neurology to psychiatry, then it all rested on an understanding of the limbic system. It should be recalled that MacLean originally envisioned the connections between the neocortex and the limbic lobe to be limited in scope (MacLean, 1955). Now we know that they are indeed massive. In all fairness, however, MacLean developed his theory 50 years ago. Classic tract-tracing studies in the late 1960s (Pandya and Kuypers, 1969; Jones and Powell, 1970) outlined a large system of cascading pathways from primary cortical sensory areas via unimodal association areas to multimodal regions in prefrontal and temporal association cortex, which in turn is closely related to both the hippocampal formation and the amygdala. More recent anatomical studies, furthermore, have shown significant connections between the limbic lobe and most surrounding neocortical areas, including the frontal lobe (Van Hoesen et al., 1993).

FIGURE 1.1 Diagram of the brain by Paul MacLean (1949) illustrating his concept of the visceral brain (shaded) and the “Papez circuit” (arrows). Abbreviations: M—mammillary body; AT—anterior thalamic nucleus. (Reprinted with permission)

Although neither Papez nor MacLean made reference to Broca in their original 1937 and 1949 papers, it is difficult to invoke the image of the cingulate and parahippocampal gyri without mentioning the great limbic lobe of Broca (1878). On the basis of extensive comparative anatomical observations, Paul Broca, like Thomas Willis (1664) before him, noticed that the cingulate gyrus (callosal gyrus) and parahippocampal gyrus (hippocampal gyrus) form a border (limbus) around the corpus callosum and brainstem. Since primary olfactory input seemed to enter both the cingulate and parahippocampal gyri, the sense of smell appeared to have an especially dominant influence on the functions of this cortical ring.¹ Although hardly ever mentioned in the literature, it is interesting to note that Broca associated the olfactory input with the emotional functions reflecting “the brute within,” thus implying a connection between the great limbic lobe and “lower instincts” related to emotions that underlie behavior. In hindsight, and with special reference to the continuing evolution of the limbic system concept, it is tempting to agree with Pozzi, who in 1888 wrote that Broca’s great limbic lobe was “perhaps Broca’s greatest claim to admiration by posterity” (referenced in Schiller, 1979).

Amygdala was not included in Papez’s original theory of emotion, but MacLean, with reference to the findings by Klüver and Bucy (1937), made amygdala one of the epicenters in a more extensive system, which he originally called the “visceral brain” (MacLean, 1949). MacLean chose the term visceral in the old-fashioned sense of strong, inward feeling (MacLean, 1978), but he soon changed the name to the more neutral term limbic system (MacLean, 1952) because of complaints from physiologists, who generally have a more narrow definition of the term visceral. MacLean, in choosing the term l...

Table of contents

• Cover image
• Title page
• Table of Contents
• PREFACE
• ABOUT LENNART HEIMER
• ACKNOWLEDGMENTS
• Chapter 1: THE LIMBIC SYSTEM; A CONCEPT IN PERPETUAL SEARCH FOR A DEFINITION
• Chapter 2: THE ERODING RELEVANCE OF THE LIMBIC SYSTEM
• Chapter 3: THE ANATOMY OF THE BASAL FOREBRAIN
• Chapter 4: THE GREATER LIMBIC LOBE
• Chapter 5: COOPERATION AND COMPETITION OF MACROSYSTEM OUTPUTS
• LITERATURE CITED
• INDEX