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Neurobiology of Compassion Mallory Taylor Geisel School of Medicine Medicine is changing. This assertion is undeniable, and has routinely been relayed to medical students, physicians, and the broader public. But another branch of this story exists that is less often told, but no less true: medicine is changing us. The healthcare system has been under society’s microscope in recent times, as the American public engages in the discussion of reform. With the passage and impending implementation of the Affordable Care Act, debates surrounding insurance coverage and physician reimbursement have dominated the news. As policymakers attempt to mend our broken system, a new component is emerging as a major contributor to its failure – damaged physicians. An unfortunate body of evidence is beginning to surface about the condition our medical students, residents, and physicians are in. Nearly half of all medical students and practicing physicians report symptoms of burnout. And the consequences of this unfortunate statistic are numerous: including increased medical error, poorer patient satisfaction, depression, and what is termed “compassion fatigue.” (Shanafelt, et al.) The degree of burnout was actually not associated with hours worked or unattained work-life balance. Instead, the only factor that was predictive of burnout risk was practicing in a primary care specialty. This correlation seems to indicate that our system level “healthcare crisis” is intimately tied to the endemic “compassion crisis” in the US. So, what can be done to address this facet of the problem? In addition to bureaucratic changes to alleviate unnecessary provider stress, new insights into the science of empathy and compassion may help us address the issue on an individual level. The neurological home of compassion Compassion, as defined by Merriam Webster, is the sympathetic consciousness of others’ distress together with a desire to alleviate it. Compassion, as defined by neurophysiologists, is the network biology of cortical and subcortical regions relevant to interoceptive and emotional processing. We can relate to the subjective feeling of wanting to help end another’s suffering, but it is a little harder to get in touch with the sensation of our neurons firing in the superior temporal sulcus. However, oftentimes the key to understanding behavior is delineating its origin, right down to the synapse. Dr. William Mobley, a trained child neurologist and co-founder of Stanford’s Center for Compassion and Altruism Research and Education, has done extensive research on the neurological correlates of empathy and compassion. His work has focused on the network of the anterior insular cortex (AIC) and anterior cingulate cortex (ACC). The AIC serves as a center for interoceptive awareness – subjective feelings, attention, choices, and intentions. Dr. Mobley has hypothesized, then, that the AIC is the seat of emotional sensory processing, or self-awareness, a key component of compassion. Neuroanatomically, the AIC shares rich connection to the ACC, which has been dubbed the ‘emotional motor system.’ Therefore, activation of the AIC in response to emotional stimuli results in concomitant activation of the ACC, which may encourage accurate and appropriate responses to those emotional stimuli. The AIC/ACC network is a unique connection. It does not exist in this form in nonhuman primates. It is also the only region containing cells called Von Economo neurons, which have recently evolved only in big-brained mammals whose environment requires social interaction. Interestingly, these neurons also selectively degenerate in Frontotemporal Dementia, a disease marked by diminished empathy. Another branch of study approaches the question from another angle: what is necessary for empathetic accuracy? Most social cognition data to this point has followed one of two fairly different paths. The first hypothesis is that shared representations (SR’s) of experienced and observed responses allow perceivers to vicariously experience what it is like to be the target of their perception. Activation of your mirror neurons in the limbic and motor regions, therefore, reproduces a similar experience in yourself that you’re observing in another, and you are able to understand their emotions. Almost literally ‘putting yourself in someone else’s shoes.’ The second path has focused on the cortical regions activated when we make specific attributions about the intentions, beliefs, and feelings of others, or mental state attribution (MSA). Brain regions recruited during MSA includes temporal and parietal regions thought to control shifts in attention to social cues, as well as medial prefrontal regions that derive MSAs from integrated combinations of semantic, contextual, and sensory inputs. These two mechanisms appear to be relatively independent, but are both indicated in the quest for interpersonal understanding. A recent study by Zaki, et al used fMRI to delineate which mechanism(s) might be at play during accurate inferences about the emotions of another. Whole-brain fMRI was collected from subjects while they watched videos of people talking and rated their perceived emotional state. This was then compared to how the taped subjects rated their own emotions while speaking. The outcome was termed emotional accuracy (EA). Not entirely surprisingly, they found that both systems of shared representation and mental status attribution were implicated. The more emotionally accurate subjects had sustained attention to targets’ verbal and nonverbal affect cues (processed by the mirror neuron system), and inferences about targets’ states based on integration of these cues (likely occurring in the medial prefrontal cortex). (Zaki, et al.) Another recent study from MGH used fMRI to explore physicians’ brains when they believed they were treating patients’ pain. They found that the same areas of the brain that are activated with the placebo effect are also activated in the brains of doctors when they believe they are relieving the suffering of their patients. Thus, successful relief of patient suffering is therapeutic for the practitioner, as well. Interestingly, those doctors who self-identified as being able to take things from another’s perspective experienced higher satisfaction during patients’ treatments. (Jensen, et al) Closing the compassion gap Now that we recognize the problem, and science is beginning to elucidate where the root of the problem may be, what (if anything) can be done? Can something like compassion be taught or improved, or are we simply born with a fixed capacity? If compassion is actually a malleable psychological component, are there real benefits to the individual and society that justify allocation of resources to its development? Many psychological interventions seek to compensate for a negative emotional state – decrease depressive symptoms, eliminate psychoses, deter pathological thought loops, etc. However, there is now growing interest in cultivating and promoting positive emotional states and qualities. Narrowing the focus on Seligman’s “Positive Psychology Movement,” there is particular interest in the idea of training the quality of compassion. An innovative consortium from Stanford University, called the Center for Compassion and Altruisim Research and Education (CCARE, mentioned above) has developed a 9-week compassion cultivation training (CCT) program. The structured program consists of a 2-hour introductory orientation, eight once-weekly 2-hour classes, and daily compassion-focused meditation exercises. Although the structure parallel’s other well-known meditation protocols (ie, Kabat-Zinn’s MindfulnessBased Stress Reduction), the CCT program is specifically focused on elucidating and cultivating one’s skills in compassion. The operational definition of compassion, according to the CCT model, is a multidimensional entity consisting of: 1) an awareness of suffering, 2) sympathetic/emotionally moved by suffering, 3) a wish to see the relief of that suffering, 4) a readiness to help relieve that suffering. Throughout the classes, students are guided through 6 steps of compassion cultivation, culminating in an integrative daily practice. A recent randomized controlled study sought to delineate the possible effects of the CCT program. A group of 100 healthy adults were randomized to either the CCT protocol or a wait list group and assessed on two self-report compassion scales. The results are compelling. Compared to wait list controls, those who completed the CCT showed significant improvement in three orientations of compassion: compassion for self, compassion for others, and compassion from others. The authors also noted that the amount of formal meditation correlated with improved compassion for others. (Jazaieri, H. et al) Another investigation in Boston used a novel empathy awareness training model rooted in neurobiology of emotions. Residents and fellows at MGH were randomized to either an intervention group or standard residency training group. Those in the intervention arm received three 60-minute classes aimed at exploring the neurobiology and physiology of empathy training, increase emotional awareness, and teach empathetic behavioral responses. The primary outcome measure was patients’ blinded scoring of their perceptions of the residents’ level of compassion and empathy before and after training. The treatment arm showed an increase in patient-rated empathy after training, with a greater change in women than in men. The control group actual showed a decline in patient empathy rating over the same time course. (Riess, et. al). This study, coupled with the aforementioned paper, indicate that compassion and empathy may in fact be a trainable skill. Although there are many intuitive and anecdotal advantages to increased compassion and empathy, supplying evidence for its objective benefits would be useful in considering implementation at a systems level. A recent study from Emory set out to answer that very question. A group of 61 healthy adults were randomized to either 6 weeks of compassion meditation training or a health discussion control group, followed by a standard laboratory stressor. Plasma IL-6 and cortisol measures, as well as scores on the Profile of Mood States questionnaire determined physiological and behavioral responses to the stressor. There were no preintervention baseline measures of these variables, but results indicated no main effect of group assignment on IL-6, cortisol, or POMS score. However, within the meditation group, increased meditation practice was significantly correlated with decreased stress-response IL-6 and POMS scores. Although these results lack a certain robustness, they may indicate that significant compassion meditation practice could reduce stress-related immune and behavioral responses. More research in these objective domains is clearly warranted. (Pace, T. et al.) Conclusions Medicine has changed. Becoming a physician in today’s healthcare environment is so vastly different from what it was in the past that it is virtually a new profession. In addition to commanding medical knowledge and clinical skill, today’s physicians must have sufficient managerial, business, and political talent to survive in an emaciated healthcare system. Coupled with these administrative strains, as a more emotionally aware society is beginning to note, are some very real psychological and personal consequences for today’s doctors. However, as we are beginning to uncover and understand these issues, more energy is also being devoted to developing solutions. And not a moment too soon, as it is becoming clear that this matter has moved beyond an optional amenity: finding ways to promote the health and happiness of physicians is a necessary component for the entire system to function. Because, a healthcare system drained of its empathetic and compassionate core simply cannot be sustained. Resources Stanford Center for Compassion and Altruism Research and Education: http://ccare.stanford.edu/ (option to join listserv, get notifications for events/conferences/lectures on website) Riess, Helen, MD. "Empathy Training for Resident Physicians: A Randomized Controlled Trial of a Neuroscience-Informed Curriculum." J Gen Intern Med 26.1 (2011): n. pag. Web. Mobley, William, MD, PhD. "Toward a Neurobiology of Empathy and Compassion for Physicians: How Do We Educate Them?" Arnold P. Gold Society Biennial Conference. Chicago. Lecture. (Slides available from Gold Society upon request) Zaki, Jamil. "The Neural Bases of Empathetic Accuracy." PNAS 106.27 (2009): 11382-1387. Pace, Thaddeus, PhD. "Effect of COmpassion Meditation on Neuroendocrine, Innate Immune and Behavioral Responses to Pyschosocial Stress."Psychoneuroendocrinology 34.1 (2009): 87-98. Jazaleri, Hooria. "Enhancing Compassion: A Randomized Controlled Trial of a Compassion Cultivation Training Program." J Happiness Stud (2012): n. pag. Web. Shanafelt, et. al. Burnout and Satisfaction With Work-Life Balance Among US Physicians Relative to the General US Population. Arch Intern Med. 2012;172(18):1377-1385) Jensen, Karen. "Sharing Pain and Relief: Neural Correlates of Physicians during Treatment of Patients." Molecular Psychiatry (2013): Advanced web publication