A. D. (Bud) Craig on the Anterior Insula and Human Awareness

Fast Moving Front Commentary, May 2011

A. D. (Bud) Craig

Article: How do you feel - now? The anterior insula and human awareness

Authors: Craig, AD
Journal: NAT REV NEUROSCI, 10 (1): 59-70, JAN 2009
Addresses: Barrow Neurol Inst, Atkinson Res Lab, Phoenix, AZ 85013 USA.
Barrow Neurol Inst, Atkinson Res Lab, Phoenix, AZ 85013 USA.

A. D. (Bud) Craig talks with ScienceWatch.com and answers a few questions about this month's Fast Moving Fronts paper in the field of Neuroscience & Behavior.

SW: Why do you think your paper is highly cited?

This 2009 paper provides a succinct overview of an extraordinarily broad range of convergent functional, anatomical, and clinical evidence regarding the insular cortex, a hidden lobe of the human brain that was poorly understood. The article is being cited frequently because activation of the insular cortex is being found in hundreds of functional imaging studies.

SW: Does it describe a new discovery, methodology, or synthesis of knowledge?

Activation of the human insular cortex occurs during virtually every feeling, emotion, perception, and behavior, and alternatively, degeneration of the anterior insula can produce loss of emotional awareness and self-conscious behaviors, most clearly in patients with fronto-temporal dementia. In this article, I suggested that the anterior insula engenders human subjective awareness, and I proposed a model for how this might occur. This proposal provides a cogent and appealing explanation for the convergent evidence that I highlighted and synthesized in this 2009 article.

SW: Would you summarize the significance of your paper in layman's terms?

The insula is physically hidden beneath the overlying folds of parietal and temporal cortex that form the Sylvian fissure, and so it has often been simply ignored. My paper describes how the insula substantializes human feelings from the body, and it highlights new evidence indicating that the insula may engender all feelings, and even awareness.

Prior to my paper, it had generally been taught that the insula is an archaic deep brain structure related to visceral function and autonomic control, that all sensations and feelings from the body involve the classical somatosensory cortex, and that human consciousness involves vast connectional networks across the entire cerebral cortex or speculative quantum mechanical interactions. To the best of my knowledge, no prior author had considered the possibility that consciousness might be engendered by a particular region of hidden cortex.

"The upcoming studies of insular function will enable deep insights into the neural basis for subjectivity, feelings, volition, individual personality, belief, and self-modulation."

More specifically, the model I proposed in this paper posits that the primary interoceptive cortex in the dorsal posterior insula provides the basis for a progressive integration of increasingly energy-efficient homeostatic re-representations extending from posterior to anterior in the insula that successively incorporate all neural activity; this integration culminates in a representation of all salient activity at each moment of present time that underpins a cinemascopic representation of the sentient self, or the "material me."

In the model, comparator buffers that enable the feelings of the present moment to be compared with those from a past moment or the anticipated feelings of a future moment provide the basis for an introspective subjectivity that cannot "see" itself, because it is always one tick late, consonant with the description of consciousness by William James. In this model, the representation of feelings in the insula (or, limbic sensory cortex) is complemented by the representation of behavioral agency in the anterior cingulate, or limbic motor cortex.

I suggested that the evolution of the homeostatic integration of all neural activity in the insula was driven by the increasing proportion of the body's energy budget that is utilized by the hominid brain (approximately 25% in adult humans, and as much as 60% in infants). This proposal is consistent with the social brain hypothesis of evolutionary hominid forebrain enlargement and with the recognition that energy utilization is a crucial arbiter of brain evolution.

This proposal provides a solid basis for new perspectives on the forebrain asymmetry of emotion, subjectivity, the emotional nature of subjective time, the emergence of music, and the high concentrations of "Von Economo neurons" that are peculiar to the anterior insula and anterior cingulate cortices of hominid primates, whales, and elephants.

SW: How did you become involved in this research, and how would you describe the particular challenges, setbacks, and successes that you've encountered along the way?

I am a functional neuroanatomist who spent years using single-unit electrophysiological and high-resolution tract-tracing methods to map a novel pathway in primates for feelings from the body, such as temperature, pain, itch, muscle ache, and so on. The terminus of this pathway in the dorsal posterior insula, which provides a primary cortical image of these affective feelings, had not been glimpsed in earlier work.

Eventually, I realized that the spinal and brainstem components of this pathway can be viewed as the long-missing sensory complement of the autonomic nervous system, and that the evolutionary appearance of the phylogenetically novel cortical projection in primates provides a high-resolution interoceptive (or homeostatic) sensory representation of the physiological condition of the body—that is, "how you feel."

Based on our original positron emission tomography (PET) imaging study of brain activation during feelings of cool temperatures, which validated this pathway in humans, I had suggested in an earlier article that integration within the insula leads to re-representations in the anterior insula that correlate with human awareness of affective feelings, consistent with the well-known James-Lange theory of emotion.

In the field of pain research, my functional anatomical findings constituted a paradigm shift that fundamentally contradicted long-standing views, and accordingly resulted in considerable resistance from leaders in the field, as well as funding difficulties. Similarly, although the model for awareness I proposed in this paper resonates with investigators across many fields, particular prominent authors who have different opinions regarding consciousness have chosen to ignore or deny these views.

SW: Where do you see your research leading in the future?

This 2009 article immediately led me to recruit authors for a "Special Issue on the Insula" in a specialized neuroscience journal, so that the leading investigators from the wide-ranging and disparate fields of neuroscience that I had highlighted could each re-appraise their fields from the new perspective afforded by the extraordinary convergence of evidence regarding the insula and the new proposals I had made.

The ideas generated by these 21 articles will certainly guide new basic and clinical studies on the neural bases of mood disorders (e.g., anxiety, depression, ADHD, PTSD), schizophrenia, somatization syndromes, risk and error processing, the forebrain bases for positive and negative emotions, decision-making, music therapy, meditation, focal attention, and so on.

In order to address the functions of the insula, new techniques will be needed that combine imaging and electrophysiological recordings at high spatial and temporal resolution, perhaps involving special patient groups, such as those who experience heightened awareness during ecstatic seizures.

SW: Do you foresee any social or political implications for your research?

The upcoming studies of insular function will enable deep insights into the neural basis for subjectivity, feelings, volition, individual personality, belief, and self-modulation. Confirmation of these ideas will unequivocally substantiate the fact that the human mind is based on the evolved capacity of our brains, and is not an extracorporeal or mystical entity.

These insights will also lead to many new discussions of very practical social matters such as the neural underpinnings of moral responsibility, legal insanity, and juvenile delinquency, as typified by the new books Brain-wise by the philosopher Patricia Churchland and The Ethical Brain by the cognitive neuroscientist Michael Gazzaniga.End

A. D. (Bud) Craig, Ph.D.
Atkinson Research Scientist
Barrow Neurological Institute
Phoenix, AZ, USA



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