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Anterior Cingulate Cortex: The Evolution of an Interface between Emotion and Cognition
John M. Allman
California Institute of Technology

In 1937 Papez proposed a linkage between cingulate cortex and emotion based on the relay of connections from the hypothalamus to the anterior thalamus and from there to the cingulate cortex. A large body of clinical and functional imaging data support the crucial role of the ventral part of anterior cingulate cortex in emotional experience. However the dorsal part of anterior cingulate cortex is equally strongly linked to cognition. There is substantial evidence from studies utilizing source-localized electroencephalography (EEG), positron emission tomography (PET), and functional magnetic resonance imaging (fMRI) that tasks requiring the solution of problems with conflicting cues strongly activate the dorsal component of anterior cingulate cortex. Moreover the activity of this area increases with task difficulty.

Recent evidence from EEG and fMRI indicates that the anterior cingulate is particularly active when the subject recognizes that he or she has just committed an error in one of these difficult tasks. Thus the anterior cingulate cortex may serve as a "reality check" necessary for successful adaptation to environmental variation.

There is some degree of overlap between the emotional and cognitive components of the anterior cingulate, and they are extensively interconnected. Some have theorized that the cingulate cortex is phylogenetically more primitive that the neocortex. However, the anatomical support for this theory is weak. The main difference between cingulate cortex and neocortex is that layer 4 is poorly developed or absent in cingulate cortex, but this is also true for parts of neocortex.

Recently my colleagues and I have found a morphologically distinct population of neurons in anterior cingulate cortex, the spindle cells, that are present only in humans and our closest relatives, the bonobos, chimpanzees, gorillas and orangutans (Nimchinsky et al,1999, Proceedings of the National Academy of Sciences, 96:5268-5273). The concentration of spindle cells declines with taxonomic distance from humans. The spindle cells were not found after an exhaustive search in 23 other species of primates or 30 species from other mammalian orders .

The spindle cells are large neurons and, unlike other nearby neurons, the volumes of their cell bodies are strongly correlated with relative brain size. Since cell volumes probably reflect the sizes of their axonal arborizations, this implies that the spindle cells may have widespread connections with other parts of the brain. EEG studies indicate that the anterior cingulate generates a distinct signal which oscillates from 4 to 7 cycles per second and that the amplitude of this signal increases with task difficulty. This signal may be involved in the coordination of brain areas in tasks requiring intense concentration and mental effort. We propose that the spindle cells might be involved in the generation of this coordinating signal.

John Allman
Division of Biology 216-76
Caltech
Pasadena, CA 91125

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