Limbic System
Rolf Kötter, in Encyclopedia of the Neurological Sciences, 2003
Multiple Definitions of Limbic System
A common view of the limbic system is limited to cortical structures (limbic cortex): The C-shaped topography of the cingulate gyrus and hippocampal region (gyrus fornicatus) is completed by Broca with olfactory tract and bulb, together forming the racket-shaped limbic lobe (Fig. 1). This concept is related to the older entity of the rhinencephalon (olfactory brain), and their proximity was reflected until recently in textbooks dealing with limbic and olfactory systems under a common heading. A modern connectivity-based concept of limbic cortex by Lopes da Silva and coworkers is equally based on the gyrus fornicatus but closes its gap with reciprocal fiber projections linking the subcallosal area with the hippocampal regions (Fig. 2).
Subcortical structures are added to the gyrus fornicatus in the classic Papez circuit consisting of hippocampus, hypothalamus, anterior thalamic nucleus, cingulate gyrus, and their interconnections. While the Papez circuit was originally proposed to form a mechanism of emotional experience and expression, most neuroscientists currently associate the amygdala with (negative) emotions but exclude the hippocampus as a nonemotional cognitive structure. The conglomerate of Broca's limbic lobe, the Papez circuit, and additional brain structures is synthesized by MacLean to the visceral brain and then renamed the limbic system as the center of neuroendocrine regulation and emotions.
In addition to affecting emotions, lesions of various limbic structures can lead to striking memory impairments. Particularly well investigated is the inability of humans and other primates to acquire new memories after extensive bilateral medial temporal lobe lesions. Other lesions to limbic structures evoke complex disorders of personality, cognition, or consciousness.
Recent attempts to establish the extent of the limbic system by more detailed cytoarchitectonics, histochemistry, connectivity studies, or electrophysiology have provided additional anatomical variety involving parts of neocortex, basal ganglia, and brainstem (specifically insular cortex, nucleus accumbens, and formatio reticularis, respectively). These observations have been conceptualized both in horizontally oriented hierarchical and in vertically oriented parallel processing models of the brain. The former is most clearly expressed in MacLean's triune brain concept of three evolutionarily stacked brain developments, where the limbic system is seen to interface the reptilian brainstem with the mammalian neocortex. Parallel processing of limbic and nonlimbic modalities in cortical as well as subcortical structures is a characteristic of the basal ganglia-thalamo-cortical loops proposed by Alexander and coworkers (Fig. 3). Perhaps the most common feature among limbic system concepts is their tendency to consider closed-loop arrangements as a morphological substrate for assumed reverberatory activity. The similarity of such concepts to ideas from cybernetics and systems theory is obvious.
Today, the term limbic may relate to a multitude of different and partly contradictory structural and functional conglomerates throughout the entire brain. Even with regard to its core structures, the emphasis shifts between cingulate gyrus, hippocampus, amygdala, hypothalamus, and brainstem. Simultaneously, most properties thought to characterize the limbic system are not unique to this system but also apply to other nonlimbic brain structures. Most strikingly, some disturbances of memory, emotional, or cognitive processes attributed to limbic system disorders are known to occur with isocortical, particularly prefrontal and parietal, lesions. “Preservation of the self and the species” is such a comprehensive concept that no part of the brain is excluded from it.
Restricted and unique definitions of the limbic system arise from adherence to a single experimental method and definitory criterion, such as cytoarchitectonical delineation of archicortex or histochemical detection of limbic system-associated protein. Assuming that remaining expert arguments about precise detection thresholds can be resolved, such investigations lead to enumerations of brain structures with poor justification of “limbic” or “system” terminology. In particular, definitions based on single structural criteria remain functionally meaningless since the hope that new methods would incorporate converging evidence of a unique limbic system have remained elusive.