Attempts to understand the effector systems that control emotional behavior have a long history. In 1937, James Papez first proposed that specific brain circuits are devoted to emotional experience and expression (much as the occipital cortex is devoted to vision, for instance). In seeking to understand what parts of the brain serve this function, he began to explore the medial aspects of the cerebral hemisphere. In the 1850s, Paul Broca had used the term “limbic lobe” to refer to the part of the cerebral cortex that forms a rim (limbus is Latin for rim) around the corpus callosum on the medial face of the hemispheres (Figure 29.3). Two prominent components of this region are the cingulate gyrus, which lies above the corpus callosum, and the hippocampus, which lies in the medial temporal lobe.

For many years, these structures, along with the olfactory bulbs, were thought to be concerned primarily with the sense of smell. Papez, however, speculated that the function of the limbic lobe might be more related to the emotions. He knew from the work of Bard and Hess that the hypothalamus influences the expression of emotion; he also knew, as everyone does, that emotions reach consciousness, and that higher cognitive functions affect emotional behavior. Ultimately, Papez showed that the cingulate cortex and hypothalamus are interconnected via projections from the mammillary bodies (part of the posterior hypothalamus) to the anterior nucleus of the dorsal thalamus, which projects in turn to the cingulate gyrus. The cingulate gyrus (and a lot of other cortex as well) projects to the hippocampus. Finally, he showed that the hippocampus projects via the fornix (a large fiber bundle) back to the hypothalamus. Papez suggested that these pathways provided the connections necessary for cortical control of emotional expression, and they became known as the “Papez circuit.”

Over time, the circuitry initially described by Papez has been revised to include parts of the orbital and medial prefrontal cortex, ventral parts of the basal ganglia, the mediodorsal nucleus of the thalamus (a different thalamic nucleus than the one emphasized by Papez), and a large nuclear mass in the temporal lobe anterior to the hippocampus, called the amygdala. This set of structures, together with the hippocampus and cingulate cortex, is generally referred to as the limbic system (Figure 29.4). Thus, whereas some of the structures that Papez originally described (the hippocampus, for example) now appear to have little to do with emotional behavior, the amygdala, which was hardly mentioned by Papez, clearly plays a major role in the experience and expression of emotional behavior (Box B).

About the same time that Papez proposed that some of these structures were important for the integration of emotional behavior, Heinrich Klüver and Paul Bucy were carrying out a series of experiments on rhesus monkeys in which they removed a large part of both medial temporal lobes, thus destroying much of the limbic system. They reported a set of abnormal behaviors in these animals that is now known as the Klüver-Bucy syndrome (Box C). Among the most prominent changes was visual agnosia: The animals appeared to be unable to recognize objects, although they were not blind, a deficit similar to that seen in human patients following lesions of the temporal cortex (see Chapter 26). In addition, the monkeys displayed bizarre oral behaviors. For instance, these animals would put objects into their mouths that normal monkeys would not. They exhibited hyperactivity and hypersexuality, approaching and making physical contact with virtually anything in their environment; most importantly, they showed marked changes in emotional behavior. Because they had been caught in the wild, the monkeys had typically reacted with hostility and fear to humans before their surgery. Postoperatively, however, they were virtually tame. Motor and vocal reactions generally associated with anger or fear were no longer elicited by the approach of humans, and the animals showed little or no excitement when the experimenters handled them. Nor did they show fear when presented with a snake—a strongly aversive stimulus for a normal rhesus monkey. Klüver and Bucy concluded that this remarkable change in behavior was at least partly due to the interruption of the pathways described by Papez. Interestingly, a similar syndrome has been described in humans who have suffered bilateral damage of the temporal lobes.

When it was later demonstrated that the emotional disturbances of the Klüver-Bucy syndrome could be elicited by removal of the amygdala alone, attention turned more specifically to the role of this structure in the control of emotional behavior.