Although the natural stimuli for emotion involve the same neocortical perceptive–cognitive mechanisms, that underlie nonemotional sensory experiences, there are important differences relating to the prominent visceral effects and particular behavioral reactions evoked by emotion. Bard, in 1928, first produced “sham rage” in cats by removing the cerebral hemispheres and leaving the hypothalamus and brainstem intact. This is a state in which the animal reacts to all stimuli with expressions of intense anger and signs of autonomic overactivity. In subsequent studies, Bard and Mountcastle found that only if the ablations included the amygdala on both sides would sham rage be produced; removal of all the neocortex, but sparing of the limbic structures resulted in the opposite state—placidity. Removal of the amygdaloid nuclei in the macaque, a normally aggressive and recalcitrant animal, greatly reduced the reactions of fear and anger (Klüver-Bucy syndrome, see further on). The precise role of the hypothalamus and amygdala in the production of both directed and undirected anger and displays of rage has turned out to be far more complex. In any case, Papez, on the basis of these and his own anatomic observations, postulated that the limbic parts of the brain elaborate the functions of central emotion and participate as well in emotional expression.
The cingulate gyrus plays a key role in the behavior of animals and humans. According to Bear, and as conceptualized by Baleydier and Mauguiere, the cingulate gyri serve dual functions in cognition and in emotional reactions. Stimulation produces autonomic effects similar to the vegetative correlates of emotion (increase in heart rate and blood pressure, dilatation of pupils, piloerection, respiratory arrest, breathholding). More complex responses, such as fear, anxiety, or pleasure, have been reported during neurosurgical stimulative and ablative procedures, although these results are inconsistent. Bilateral cingulectomies performed in the past on psychotic and anxious patients result in an overall diminution of emotional reactions (Ballantine et al; Brown). Some investigators believe that the cingulate gyri are also involved in memory processing (functioning presumably in connection with the mediodorsal thalamic nuclei and mediotemporal lobes) and in exploratory behavior and visually focused attention. In humans, this system appears to be more efficient in the nondominant hemisphere.
Another aspect of limbic function has come to light with information about the neurotransmitters that interconnect the structures within the system. The concentration of norepinephrine is highest in the hypothalamus and next highest in the medial parts of the limbic system; at least 70 percent of this monoamine is concentrated in terminals of axons that arise in the medulla and in the locus ceruleus of the rostral pons. Serotonin is a major transmitter for neurons originating in the reticular formation of the midbrain whose axons terminate in the amygdala septal nuclei, and lateral parts of the limbic lobe. The axons of neurons in the ventral tegmental parts of the midbrain, which ascend in the medial forebrain bundle and the nigrostriatal pathway, contain a high content of dopamine. Perhaps this explains the observation that a severe depressive reaction may be produced by electrical stimulation of the substantia nigra with an aberrantly placed electrode for the treatment of Parkinson disease (see Chap. 38).