Thursday, December 14, 2017

Von Economo Neurons: The Neural Basis for Self-Awareness, Social Awareness, and the Moral Sense?

In the summer of 1996, I participated in a Summer Institute on the Biology of Human Nature at Dartmouth College, directed by Roger Masters and Robert Perlman.  At the time, I was finishing my book manuscript Darwinian Natural Right: The Biological Ethics of Human Nature; and this Summer Institute helped me think through many of the questions for the book, including the fundamental question of the biological basis for the human mind and morality.

We spent one afternoon at a human dissection lab at Dartmouth Medical School, where a professor of neurology guided us in our dissection of two human brains.  We talked about how the human brain compares with the brains of other animals.  And we asked what might make the human brain unique.  As we sliced up these brains, I remember asking myself: Where's the soul?  How does the soul or mind arise in the evolution of the brain?

At one point, the neurology professor suggested that part of the answer as to the uniqueness of the human brain might be special neurons--particularly, "spindle neurons" that seem to facilitate fast communication across distant neural networks in the large human brain, neurons that are found only in certain areas of the human brain and possibly in some other primate brains.  Looking back on this, I assume that the professor had read a recently published article on spindle neurons in the human anterior cingulate cortex (Nimchinsky et al. 1995).

I was intrigued by this, and I wanted to learn more.  But as far as I could tell, there wasn't much research on these spindle neurons.  Only recently, have I discovered that over the past 15 years there has been intense study of these neurons.  Although the conclusions remain very speculative, there is evidence that these neurons provide some of the neural basis for human self-awareness, social awareness, and the moral sense.

As I have often argued on this blog--most recently in response to Roger Scruton's claim that biological science cannot study the human mind--this sort of research shows how evolutionary biologists can explain the evolutionary emergence of the human mind in the primate brain and body, although the inward experience of subjective self-awareness will always remain somewhat mysterious.

A Cartoon of Von Economo (Spindle) Neurons with Only a Single Dendrite Compared with Pyramidal Neurons with Many Dendrites

The mystery is that while each of us has direct access to our own subjective consciousness, we cannot directly observe the conscious experience of anyone else.  So when neuroscientists put someone in a functional MRI brain scanning machine, the scientists can see what parts of the brain light up in the brain images as indicating neural activity, but they cannot see what the person is thinking or feeling, and so they must ask that person to report what he or she was thinking or feeling. The scientists can then infer that the observed patterns of neural activity are somehow correlated with the reported thoughts and feelings.

Scientists have observed that the anterior insular cortex (AIC) and the anterior cingulate cortex (ACC) on both sides of the brain are jointly active in most functional imaging studies, and that the AIC supports emotional feelings, self-awareness, and social awareness.  Moreover, they have observed that these two parts of the brain have a high concentration of spindle neurons that are not found anywhere else in the brain, except for small numbers in the dorsolateral prefrontal cortex.

Spindle neurons are also called von Economo neurons (VENs), because Constantin von Economo provided the first comprehensive description of these neurons in 1925 (Seeley et al. 2012).  It was not until the end of the 20th century, however, that comparative neurologists began to study VENs as special neurons that might be part of what explains the evolutionary uniqueness of the human mind.

VENs appear in the brains of only a few species.  They are present in gorillas, bonobos, chimpanzees, and orangutans, although in numbers smaller than for humans.  They are also found in the brains of whales, dolphins, and elephants.  Thus, VENs are associated with species that have large brains, which suggests the possibility that VENs facilitate speedy communication of neural signals over neural networks scattered over large brains.  VENs are also associated with species that have complex social lives and that show mirror self-awareness (recognizing themselves in mirrors).  This supports the speculation that VENs allow animals to self-consciously navigate successfully through complex social interactions.  This fits with the "social brain hypothesis" of Robin Dunbar--the idea that the evolution of large and complex brains arose primarily as an adaptation for the mental challenges of social life (Allman et al. 2010; Bauernfeind et al. 2013; Cauda et al. 2014; Chen 2009; Craig 2015, pp. 217-19; Dunbar and Shultz 2007).  (I have written a post on Dunbar's presentation of his theory at the 2013 conference of the Mont Pelerin Society in the Galapagos Islands.)

Allman et al. (2010, pp. 496-97) have argued that the VENs in the anterior insula and anterior cingulate cortex are activated either by social error--by some defect in an individual's social network--or by social success--by some satisfying experience in a social network:
". . . For example, these structures are activated by resentment (Sanfey et al. 2003), deception (Spence et al. 2001), embarrassment (Berthoz et al. 2002), and guilt (Shin et al. 2000).  They are also activated by feelings of empathy for the suffering of others, another type of social error signal (Singer et al. 2004).  In mothers, FI in the right hemisphere responds to the crying of distressed infants (Lorberbaum et al. 2002), which is a powerful social error signal.  The anterior insula (including both superior and inferior components) was activated when partners in the prisoner's dilemma game failed to reciprocate cooperative moves made by the subject, which is a type of social error signal (Rilling et al. 2008).  Anterior insula and anterior cingulate cortex are also activated by pro-social signals, such as love and trust (Bartels and Zeki 2004; Singer et al. 2004), which suggests that these structures register both negative and positive aspects of the states of social networks.  The responses of FI and LA are parametrically related to how humorous subjects judge cartoons to be; the humorous content of the cartoons typically involved social errors (Watson et al. 2007)."
Here the VENs are associated with the moral emotions of social life such as guilt, shame, resentment, sympathy, love, and a sense of humor.

There are few VENs in human infants at birth.  The number of VENs increases rapidly during the first eight months of life, and they reach adult numbers at about four years of age.  The number is extremely variable between individuals, which might explain individual variability in the acuteness of self-awareness and social awareness (Allman et al. 2011).

Another way to infer the functional activity of VENs is to notice how the degeneration of VENs leads to distinctive kinds of mental disorders.  For example, early behavioral variant frontotemporal dementia arises from the degeneration of VENs in the anterior insular cortex and the anterior cingulate cortex.  People with frontotemporal dementia suffer a breakdown in their social character, showing a loss of self-conscious emotional control, social empathy, and emotional self-awareness.  They become insensitive, erratic, and irresponsible in ways that can destroy their social lives by breaking up their family lives and their professional careers.  This can be seen as additional evidence for seeing the evolution of VENs in humans as part of the evolution of the social brain (Kim et al. 2012).

Seeing people with severe forms of mental disorder like frontotemporal dementia is disturbing, because it raises the question of whether they have lost their souls, from having lost the neural activity that supports the self-awareness, social awareness, and moral sense that constitute the healthy human mind.

VENs seem to be a crucial part of that neural activity, and therefore the evolution of VENs must be part of the emergent evolution of the mind in the primate brain.

Some of my other posts on the evolution of the mind can  be found hereherehere, and here.

Most of the research that I have reported here relies heavily on brain imaging.  I have argued against the fallacy of seeing brain imaging as mind reading herehere, and here.


Allman, John, et al. 2010. "The von Economo Neurons in Frontoinsular and Anterior Cingulate Cortex in Great Apes and Humans." Brain Structure and Function 214:495-517.

Allman, John, et al. 2011. "The von Economo Neurons in the Frontoinsular and Anterior Cingulate Cortex." Annals of the New York Academy of Sciences 1225:59-71.

Bartels, A., and S. Zeki. 2004. "The Neural Correlates of Maternal and Romantic Love." Neuroimage 21:1155-1166.

Bauernfeind, Amy L., et al. 2013. "A Volumetric Comparison of the Insular Cortex and Its Subregions in Primates." Journal of Human Evolution 64:263-79.

Berthoz, S., et al. 2002. "An fMRI Study of Intentional and Unintentional (Embarrassing) Violations of Social Norms." Brain 125:1696-1708.

Cauda, Franco, et al. 2013. "Functional Anatomy of Cortical Areas Characterized by Von Economo Neurons." Brain Structure and Function 218:1-20.

Chen, Ingfei. 2009. "Brain Cells for Socializing." Smithsonian Magazine, June 2009.

Craig, Arthur D. (Bud). 2015. How Do You Feel? An Interoceptive Moment with Your Neurobiological Self. Princeton, NJ: Princeton University Press.

Dunbar, Robin, and S. Shultz. 2007. "Evolution in the Social Brain." Science 317:1344-1347.

Kim, Eun-Joo, et al. 2012. "Selective Frontoinsular von Economo Neuron and Fork Cell Loss in Early Behavioral Variant Frontotemporal Dementia." Cerebral Cortex 22:251-59.

Lorberbaum, J.P., et al. 2002. "A Potential Role for Thalamocingulate Circuitry in Human Maternal Behavior." Biological Psychiatry 51:431-45.

Nimchinsky, E. A., et al. 1995. "Spindle Neurons of the Human Anterior Cingulate Cortex." Journal of Comparative Neurology 355:27-37.

Rilling, J., et al. 2008. "Neural Correlates of the Affective Response to Unreciprocated Cooperation." Neuropsychologia 46:1265-1266.

Sanfey, A. G., et al. 2003. "The Neural Basis of Economic Decision-Making in the Ultimatum Game." Science 300:1755-1758.

Seeley, William W., et al. 2012. "Distinctive Neurons of the Anterior Cingulate and Frontoinsular Cortex: A Historical Perspective." Cerebral Cortex 22:245-50.

Shin, L. M., et al. 2000. "Activation of Anterior Paralimbic Structures During Guilt-Related Script-Driven Imagery." Biological Psychiatry 48:43-50.

Singer, T., et al. 2004. "Brain Responses to the Acquired Moral Status of Faces." Neuron 41:653-62.

Spence, S. A., et al. "Behavioural and Functional Anatomical Correlates of Deception in Humans." NeuroReport 12:2849-2853.

Watson, K. K., et al. 2007. "Brain Activation During Sight Gags and Language-Dependent Humor." Cerebral Cortex 17:314-24.


Roger Sweeny said...

There are few VENs in human infants at birth. The number of VENs increases rapidly during the first eight months of life, and they reach adult numbers at about four years of age. The number is extremely variable between individuals, which might explain individual variability in the acuteness of self-awareness and social awareness (Allman et al. 2011).

Which leads to some obvious questions. Do people with autism have substantially fewer VENs than people without? Do people with more severe autism have fewer VENs than people with less severe autism? Do people with different kinds or degrees of autism have different distributions of VENs?

Larry Arnhart said...

What little work has been done on this is confusing.

Allman et al. (2005) have proposed that autism might be caused by a failure of VENs to develop normally. But Santos et al. (2011) examined the postmortem brains of four young patients with autism and three comparably aged controls. The brains of the autism patients actually had a higher ratio of VENs to pyramidal neurons than control subjects. They surmise that patients with autism might actually suffer from too much self-consciousness/interoception!

Allman et al. 2005. "Intuition and Autism: A Possible Role for Von Economo Neurons." TRENDS IN COGNITIVE SCIENCES 9:367-73.

Santos et al. 2011. "Von Economo Neurons in Autism: A Stereologic Study of the Frontoinsular Cortex in Children." BRAIN RESEARCH 1380:206-217.