Macaque interoceptive network

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Chapter 12 endnote 4, from How Emotions are Made: The Secret Life of the Brain by Lisa Feldman Barrett.
Some context is:

The macaque [interoceptive] network is structured to function by prediction in the same way that the human network does. [...] More generally, macaque and human brains are very similar to one another, with a few notable changes, mostly at the front of the brain...

Macaques and humans both share the more ventral aspect of the interoceptive network (for body-budgeting and prediction), but humans (and not macaques) have a fully developed dorsal aspect.[1] I hypothesize that this dorsal aspect is important for helping to select which prediction errors are reliable and relevant (and therefore should be learned) vs. those that can be safely ignored.[2]

Of course, network structure is not the only thing that counts. It’s also important to consider the size and organization of brain regions.

There is a disagreement as to whether the ventral portion of the anterior insula is similar in macaques and humans or whether it has expanded uniquely in humans. The neuroanatomist Bud Craig observes that in humans, the insula increased in size relative to macaques. The increase in size is predicted by the overall increase in brain size, which correlates with increases in body size, i.e., the increase in insula size was allometric. This means that the insula increase was is not special to humans in any way. Although the insula did not increase in relative size, the difference between the ventral anterior insula in humans and macaques in absolute size was larger than for any other brain region, including regions of prefrontal cortex.[3] Craig believes this is because there is a part of the ventral anterior insula that is unique in humans and great apes, whereas other scientists see more similarities between the ventral anterior insula in humans and macaques; at least where connectivity is concerned, my lab’s findings tend to support this latter view.

Craig bases his argument on the observation that in humans and great apes, this portion of the ventral anterior insula includes broad clusters of particularly large spindle shaped neurons in Layer 5 (among the pyramidal neurons usually found in that layer) called Von Economo neurons (they have also been identified in the anterior cingulate cortex[4]). At first it was assumed that these neurons only appeared in humans and great apes,[5][6][7] but other researchers have observed similar neurons in the anterior insula of macaques monkey,[3][8] although not in large concentrated groupings. Some scientists speculate that Von Economo neurons play a special role in creating the social and emotional differences between humans and other primates,[5][9][10][11] although this hypothesis awaits scientific testing. Currently, no study has ever been published that indicates the transmission speed, neurotransmitters, axonal or dendritic distributions of Von Economo neurons gives them special functional properties.

Von Economo neurons have also been identified in other large-brained mammals, such as whales,[12] elephants,[13] baboons and lemurs,[14] as well as in the pygmy hippopotamus, the Atlantic walrus, and Florida manatee.[15] Given that there is currently no agreed upon function of these neurons, and no one knows for sure if their function changes when they are found in high concentrations, so it is not clear if this constitutes a distinct anatomical feature with functional consequences.


Notes on the Notes

  1. Touroutoglou, A., Bliss-Moreau, E., Zhang, J., Mantini, D., Vanduffel, W., Dickerson, B A., & Barrett, L. F.  (2016).  A ventral salience network in the Macaque brain.  Neuroimage, 132, 190-197.
  2. Barrett, Lisa Feldman. 2017. "The theory of constructed emotion: an active inference account of interoception and categorization." Social Cognitive and Affective Neuroscience 12 (1): 1-23.
  3. 3.0 3.1 Bauernfeind, Amy L., Alexandra A. de Sousa, Tanvi Avasthi, Seth D. Dobson, Mary Ann Raghanti, Albert H. Lewandowski, Karl Zilles et al. 2013. "A volumetric comparison of the insular cortex and its subregions in primates." Journal of Human Evolution 64 (4): 263-279.
  4. von Economo, C. 1926. "Eine neue Art Spezialzellen des Lobus cinguli und Lobus insulae." Zeitschr. Ges. Neurol Psychiatr (Berlin) 100: 706–712.
  5. 5.0 5.1 Allman, John M., Karli K. Watson, Nicole A. Tetreault, and Atiya Y. Hakeem. 2005. "Intuition and autism: a possible role for Von Economo neurons." Trends in Cognitive Sciences 9 (8): 367-373.
  6. Nimchinsky, Esther A., Emmanuel Gilissen, John M. Allman, Daniel P. Perl, Joseph M. Erwin, and Patrick R. Hof. 1999. "A neuronal morphologic type unique to humans and great apes." Proceedings of the National Academy of Sciences 96 (9): 5268-5273.
  7. Ngowyang, G. 1932. "Beschreibung einer Art von Spezialzellen in der Inselrinde-zugleich Bemerkungen über die v. Economoschen Spezialzellen." Journal fuer Psychologie und Neurologie 44: 671-674.
  8. Evrard, Henry C., Thomas Forro, and Nikos K. Logothetis. 2012. "Von Economo neurons in the anterior insula of the macaque monkey." Neuron 74 (3): 482-489.
  9. Allman, John M., Nicole A. Tetreault, Atiya Y. Hakeem, Kebreten F. Manaye, Katerina Semendeferi, Joseph M. Erwin, Soyoung Park, Virginie Goubert, and Patrick R. Hof. 2010. "The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans." Brain Structure and Function 214 (5-6): 495-517.
  10. Allman, John M., Nicole A. Tetreault, Atiya Y. Hakeem, Kebreten F. Manaye, Katerina Semendeferi, Joseph M. Erwin, Soyoung Park, Virginie Goubert, and Patrick R. Hof. 2011. "The von Economo neurons in the frontoinsular and anterior cingulate cortex." Annals of the New York Academy of Sciences 1225 (1): 59-71.
  11. Allman et al., 2011b [full reference to be provided]
  12. Hof, Patrick R., and Estel Van Der Gucht. 2007. "Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae)." The Anatomical Record 290 (1): 1-31.
  13. Hakeem, Atiya Y., Chet C. Sherwood, Christopher J. Bonar, Camilla Butti, Patrick R. Hof, and John M. Allman. 2009. "Von Economo neurons in the elephant brain." The Anatomical Record 292 (2): 242-248..
  14. Rose, M. 1928. "Die inselrinde des menschen und der tiere." Journal fuer Psychologie und Neurologie 37: 467-624. Cited in Nieuwenhuys, Rudolf. 2012. "The insular cortex: A review." In Progress in Brain Research, Volume 195: Evolution of the Primate Brain From Neuron to Behavior, edited by Michel A. Hofman and Dean Falk, 123-164. New York: Elsevier.
  15. Butti, Camilla, and Patrick R. Hof. 2010. "The insular cortex: a comparative perspective." Brain Structure and Function 214 (5-6): 477-493.