Cortical pathways to the mammalian amygdala
Section snippets
IntroductionHis operation on Benson was directed toward a specific part of the brain, the limbic system. It was a very old part of the brain, in terms of evolution. . . . It controlled the most primitive behavior—anger and fear, lust and hunger, attack and withdrawal. Reptiles like crocodiles had little else to direct their behavior. Man, on the other hand, had a cerebral cortex.
But the cerebral cortex was a recent addition. . . . The cortex had grown up around the limbic brain, which remained . . . embedded deep inside the new cortex. That cortex, which could feel love, and worry about ethical conduct, and write poetry, had to make an uneasy peace with the crocodile brain at its core. Sometimes, as in the case of Benson, the peace broke down, and the crocodile brain took over intermittently. (Michael Crichton, The Terminal Man).
His operation on Benson was directed toward a specific part of the brain, the limbic system. It was a very old part of the brain, in terms of evolution. . . . It controlled the most primitive behavior—anger and fear, lust and hunger, attack and withdrawal. Reptiles like crocodiles had little else to direct their behavior. Man, on the other hand, had a cerebral cortex.
But the cerebral cortex was a recent addition. . . . The cortex had grown up around the limbic brain, which remained . . . embedded deep inside the new cortex. That cortex, which could feel love, and worry about ethical conduct, and write poetry, had to make an uneasy peace with the crocodile brain at its core. Sometimes, as in the case of Benson, the peace broke down, and the crocodile brain took over intermittently. (Michael Crichton, The Terminal Man).
These musings about the relationship of the cerebral cortex to the limbic system are actually the thoughts of a fictional character, Dr. John Ellis, a neurosurgeon in Michael Crichton's novel entitled “Terminal Man” (Crichton, 1972). Ellis had surgically implanted a remotely controlled stimulating electrode in the amygdala of Harry Benson, a patient with temporal lobe epilepsy, in an attempt to control sporadic episodes of violent behavior. Crichton's idea for the novel was inspired by the
General considerations
The primate amygdala is located in the anteromedial part of the temporal lobe, where it lies ventromedial to the striatum and anterior to the ventral portion of the hippocampal formation (Fig. 1E). It has a similar position in nonprimates, such as the rat and cat, in which the temporal lobe is not as well developed (Fig. 2E, Fig. 3C). The amygdala in all mammals is anatomically complex (Koikegami, 1963; Price et al., 1987), consisting of numerous nuclei that often merge with their neighbors, as
Amygdalar projections to subcortical regions involved in behavior and emotion
An understanding of the significance of cortico-amygdalar projections requires a knowledge of the functional anatomy of the amygdala. As mentioned previously, stimulation of the amygdala in humans produces emotional responses that are often associated with complex experiential hallucinations. The most common emotional response elicited is fear, although rage, and occasionally pleasurable feelings, may also be produced. Stimulation and ablation studies in experimental animals have shown that the
Neuroanatomical methods
Since this review focuses on the connections of the amygdala as revealed by experimental tract tracing techniques, it is of interest to briefly review these methods. There are two major classes of tract tracing methods, anterograde and retrograde.
Projections from the olfactory bulb in primates
Anterograde tract tracing studies have shown that the macaque monkey amygdala receives projections from both the olfactory bulb and the primary olfactory cortex of the piriform lobe (Carmichael et al., 1994; Turner et al., 1978) (Fig. 5A). The primary olfactory cortex, which is defined as those cortical areas which receive direct projections from the olfactory bulb, is comprised of several regions that form a continuous zone in the vicinity of the lateral olfactory tract (LOT), the main
Anatomy of the parietal and insular lobes of primates
The primary somatosensory cortex (SI; area 3, 1, and 2) in the monkey brain, as in humans, is located posterior to, and within, the central sulcus (Fig. 1). The intraparietal sulcus of the posterior parietal region separates the superior parietal lobule (area 5) from the inferior parietal lobule (area 7). Ventral to SI and area 7 is the second somatosensory cortex (SII). It is located on the inner face of the parietal operculum on the upper bank of the lateral (sylvian) fissure (Fig. 7). SII is
Anatomy of the occipital and temporal lobes of primates
The primate occipital lobe consists of numerous retinotopically-organized visual cortical areas (Van Essen, 1985). The largest is V1, the primary visual area, which occupies the occipital pole and most of the medial and lateral aspects of the occipital lobe (Fig. 1 and Fig. 16). On the lateral surface of the hemisphere, V1 approaches the lunate and inferior occipital sulci, where it is replaced by area V2 (Fig. 16). Just anterior to V2 is area V3, which is largely concealed within the depths of
Anatomical and functional aspects of the hippocampal and rhinal cortices
Studies in primates have shown that long-term declarative memory (i.e., memory of facts and events) is critically dependent on a series of adjacent structures located in the inferomedial portion of the temporal lobe that comprise the medial temporal lobe memory system (MTLMS) (Squire and Zola-Morgan, 1991). These structures include the perirhinal cortex (PRC; located along the fundus and lateral bank of the rhinal sulcus), the entorhinal cortex (ERC; located medial to the rhinal sulcus), the
Prefrontal projections to the amygdala in primates
The frontal lobe of the monkey, like that of humans, is the portion of the cerebral cortex located anterior to the central sulcus (Fig. 1). The primary motor area (area 4) and premotor/supplementary motor area (area 6) are located between the central and arcuate sulci. The prefrontal cortex (PFC), which may be defined as the cortical projection field of the mediodorsal thalamic nucleus (Rose and Woolsey, 1948), consists of all frontal areas located anterior to the arcuate sulcus. Thus, the PFC
Summary and conclusions
Anatomical and physiological studies performed during the last 50 years have demonstrated that the amygdala is a unique subcortical structure which receives sensory information from the sensory cortices of all of the major sensory modalities. Olfactory and gustatory/visceral information has access to the amygdala at an earlier stage of cortical processing than visual, auditory and somatosensory information. Thus, olfactory inputs arise from the olfactory bulb and primary olfactory cortex
Acknowledgements
The author is grateful for the excellent assistance of Janice Burns in preparing the manuscript and Neda Ostermann in preparing the photomicrographs. I would also like to thank Drs. Martin Cassell (University of Iowa) and Joseph LeDoux (New York University) for their valuable comments on an earlier version of this manuscript. This work was supported by NIH Grant NS19733.
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