Criticisms of the limbic system concept

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Chapter 8 endnote 28, from How Emotions are Made: The Secret Life of the Brain by Lisa Feldman Barrett.
Some context is:

Scientists inspired by the classical view have claimed to localize many different emotions to limbic brain regions, such as the amygdala, that are (allegedly) under the control of the cortex and cognition. Modern neuroscience, however, has shown that the so-called limbic system is a fiction, and experts in brain evolution no longer take it seriously, let alone consider it a system.

From its very inception, the limbic system concept was criticized on both anatomic and functional grounds.[1][2][3][4][5][6][7][8][9][10] I have summarized these concerns, as follows:

  • To date, no one has succeeded in providing a generally accepted definition of what is in, and what is not in, the limbic system. There are no anatomical criteria for deciding which tissue belongs to a "limbic system" and which does not. Using connectivity as a criterion, it could be claimed that the "limbic system" includes the entire brain. Using the arrangement of neurons does not work on its own, because regions that are important for body-budgeting have many different neural organizations (subcortical clumps called nuclei; allocortical structures like the hippocampus; agranular cerebral cortex like portions of the anterior cingulate cortex; and dysgranular cortex like the medial prefrontal cortex). There are no functional criteria either. Even defining limbic regions as "the visceral brain" does not solve this problem because all animals utilize sensory inputs, past experience, and somatomotor control, in the service of body-budget control to mount motivated responses to the world. The psychologist Karl Pribram made the observation that the entire brain could be considered the visceral brain in a very real sense.
  • The regions that are conventionally placed into the so-called limbic system are not unique for emotion or motivation. For example, the hippocampus is conventionally considered to play a key role in memory. Patient HM, who had bilateral removal of key regions of limbic circuitry such as the medial temporal lobes (including the amygdala and hippocampus), had deficits in episodic memory but not in emotion or feeling;[11] it was recently discovered that HM also had a lesion in orbitofrontal cortex (also usually considered limbic tissue). In fact, within neuroscience textbooks, many different phenomena are linked to limbic tissue, including memory, attention, perception and even consciousness.
  • Limbic circuitry is not necessary for emotion. See the case of Roger, who lost his limbic circuitry to herpes simplex virus Type 1 encephalitis (HSE) yet still experiences affect.
  • It is neither anatomically nor functionally justified to separate somatomotor and visceromotor (body-budgeting) functions; nor to discuss the central and peripheral nervous systems as if they are distinct and separable systems. These are historical distinctions, not scientific ones.

Kotter & Meyer (1992)[6] call the limbic system concept "a non-empirical explanatory concept for poorly understood brain functions" (p. 105).

Brodal (1975),[2] an outspoken critic of the limbic system concept, described it as substituting magical naming for understanding — a criticism that is frequently leveled against faculty psychology.

Notes on the Notes

  1. Brodal, Alf. 1969. Neurological Anatomy in Relation to Clinical Medicine. Oxford University Press.
  2. 2.0 2.1 Brodal, Alf. 1975. "The 'wiring patterns' of the brain: neuroanatomical experiences and their implications for general views of the organization of the brain." In The Neurosciences: Paths of Discovery, I, edited by Frederic G. Worden, Judith P. Swazey, and George Adelman, 123-142. Boston, Massachusetts: Birkhäuser.
  3. Brodal, Alf. 1981. Neurological Anatomy, Oxford University Press, New York.
  4. Heimer, Lennart, and Gary W. Van Hoesen. 2006. "The limbic lobe and its output channels: implications for emotional functions and adaptive behavior." Neuroscience & Biobehavioral Reviews 30 (2): 126-147.
  5. Kaada, B. R. 1960. "Cingulate, posterior orbital, anterior insular and temporal pole cortex." Handbook of Physiology 2: 1345-1372.
  6. 6.0 6.1 Kötter, Rolf, and Niels Meyer. 1992. "The limbic system: a review of its empirical foundation." Behavioural Brain Research 52 (2): 105-127.
  7. Ledoux, Joseph. 1991. "Emotion and the limbic system concept." Concepts in Neuroscience 2: 169-199.
  8. Pribram, 1952 [full reference to be provided]
  9. Swanson, 1987 [full reference to be provided]
  10. McGaugh, 2002 [full reference to be provided]
  11. Scoville, William Beecher, and Brenda Milner. 1957. "Loss of recent memory after bilateral hippocampal lesions." Journal of Neurology, Neurosurgery & Psychiatry 20 (1): 11-21.