Social Intelligence: The New Science of Human Relationships
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Chapter 5. The Neuroanatomy of a Kiss
1. The OFC has been called the “ultimate neural integrating convergence zone.” Among the key brain areas with strong connections to the OFC are the dorsolateral prefrontal cortex, regulating attention; the sensory cortex, for perception; the somatosensory cortex and brain stem, for sensations within the body; the hypothalamus, the brain’s neuroendocrine center that regulates hormones throughout the body; the autonomic nervous system, controlling bodily functions like heart rate and digestion; the medial temporal lobe, for memory; the association cortex, for abstract thought; and brain stem centers like the reticular formation, which regulates levels of arousal in the brain. For functions of the OFC and connecting brain structures, see, for example, Allan Schore, Affect Regulation and the Origin of the Self: The Neurobiology of Emotional Development (Hillsdale, N.J.: Erlbaum, 1994); Simon Baron-Cohen, Mindblindness: An Essay on Autism and Theory of Mind (Cambridge, Mass.: MIT Press, 1995); Antonio Damasio, Descartes’ Error: Emotion, Reason and the Human Brain (New York: Grosset/Putnam, 1994).
2. The orbitofrontal region (Brodmann’s areas 11, 12, 14, and 47) regulates a wide range of social behavior. It has rich connections to the amygdala, the anterior cingulate cortex, and the somatosensory areas. Another linked cortical area is the temporal lobe, crucial for identifying what an object is, or the significance of things. All these areas play roles in coordinating smooth social interactions. The orbitofrontal lobe has an extensive network of projections throughout the emotional centers, allowing it to modulate emotional responses. One of the primary functions of these networks during a social interaction seems to be inhibiting emotional reactions, coordinating them with inputs about the social moment to make our responses well tuned. See, for example, Schore, Affect Regulation. See also Jennifer S. Beer et al., “The Regulatory Function of Self-conscious Emotion: Insights from Patients with Orbitofrontal Damage,” Journal of Personality and Social Psychology 85 (2003), pp. 594–604; Jennifer S. Beer, “Orbitofrontal Cortex and Social Behavior: Integrating Self-monitoring and Emotion-Cognition Interactions,” Journal of Cognitive Neuroscience 18 (2006), pp. 871–80.
3. The OFC connects directly to the autonomic system, making it a control center for bodily arousal and relaxation. Other cortical areas with autonomic projections include the anterior cingulate cortex and the medial prefrontal cortex.
4. During moments of motherly love the OFC essentially swamps other areas of the brain, presumably triggering a flood of warm thoughts. See Jack B. Nitschke et al., “Orbitofrontal Cortex Tracks Positive Mood in Mothers Viewing Pictures of Their Newborn Infants,” NeuroImage 21 (2004), pp. 583–92.
5. On first impressions, see Michael Sunnafrank and Artemio Ramirez, Jr., “At First Sight: Persistent Relationship Effects of Get-Acquainted Conversations,” Journal of Social and Personal Relationships 21, no. 3 (2004), pp. 361–79. Not surprisingly, the partner who is less drawn to the other has the most power in determining whether a friendship will blossom. If one person wants to connect while the other does not, the reluctant one has veto power. In other words, if you don’t want to be my friend, I can’t make you. Two factors that would intuitively seem to matter did not: initial attraction and a feeling of similarity.
6. The ACC is involved in a range of functions, notably guiding attention, sensing pain, noting errors, and regulating internal organs like breathing and heart rate. This part of the cortex has rich connections to emotional centers, such as the amygdala, lower in the brain; some neuroanatomical researchers speculate the ACC evolved as an interface connecting our thoughts with our feelings. This intertwining gives the ACC a key role in social awareness.
7. On spindle cells, see John M. Allman et al., “The Anterior Cingulate Cortex: The Evolution of an Interface Between Emotion and Cognition,” Annals of the New York Academy of Sciences 935 (2001), pp. 107–17.
8. While most all the hundreds of types of neurons in the human brain are found in other mammals, spindle cells are a rare exception. We share them only with our closest cousins, the apes. Orangutans, a distant relative, have a few hundred; our closer genetic relatives the gorillas, chimps, and bonobos have far more. And we humans have the most, close to a hundred thousand of them.
9. See A. D. Craig, “Human Feelings: Why Are Some More Aware Than Others,” Trends in Cognitive Sciences 8 (2004), pp. 239–41.
10. On ACC and social insight, see R. D. Lane et al., “Neural Correlates of Levels of Emotional Awareness: Evidence of an Interaction Between Emotion and Attention in the Anterior Cingulate Cortex,” Journal of Cognitive Neuroscience 10 (1998), pp. 525–35. People who are so chronically depressed that medications do not help them typically have unusually little activity in the ACC.
11. On social emotions, see Andrea Bartels and Semir Zeki, “The Neural Basis of Romantic Love,” NeuroReport 17 (2000), pp. 3829–34. Area F1 of the OFC and area Z4 of the ACC are rich in spindle cells.
12. On the ACC and OFC in social judgment, see Don M. Tucker et al., “Corticolimbic Mechanisms in Emotional Decisions,” Emotion 3, no. 2 (2003), pp. 127–49.
13. Tanya Chartrand and John Bargh, “The Chameleon Effect: The Perception-Behavior Link and Social Interaction,” Journal of Personality and Social Psychology 76 (1999), pp. 893–910.
14. The ACC may be only one region among many involved in a widely distributed liking-loathing neural system. Other candidates include the insula.
15. Henry James, The Golden Bowl (1904; New York: Penguin, 1987), pp. 147–49.
16. On the “people circuits,” see J. P. Mitchell et al., “Distinct Neural Systems Subserve Person and Object Knowledge,” Proceedings of the National Academy of Sciences 99, no. 23 (2002), pp. 15238–43. The neural circuits that activate during judgments about people: dorsal and ventral aspects of the medial prefrontal cortex, right intraparietal sulcus, right fusiform gyrus, left superior temporal and medial temporal cortex, left motor cortex, and regions of the occipital cortex. The three that are activated while the brain is at rest: dorsal and ventral aspects of the medial prefrontal cortex, and areas of the intraparietal sulcus.
17. Matthew Lieberman is director of the Social Cognitive Neuroscience Laboratory at UCLA. In 2001 he and Kevin Ochsner scored an unheard-of professional coup. An article they had written as lowly graduate students at Harvard was accepted in psychology’s most prestigious journal, The American Psychologist, one where even famed professors can have a tough time getting published. Their article proclaimed the joining of social psychology, cognitive science, and brain studies, launching a major strand in social neuroscience. Lieberman will be the editor of that discipline’s first scholarly journal, Social, Cognitive, and Affective Neuroscience, set to launch sometime in 2006.
18. On the default activity, see Marco Iacoboni et al., “Watching Social Interactions Produces Dorsomedial Prefrontal and Medial Parietal BOLD fMRI Signal Increases Compared to a Resting Baseline,” NeuroImage 21 (2004), pp. 1167–73.
19. On emotions as the brain’s value system, see, for example, Daniel J. Siegel, The Developing Mind: How Relationships and the Brain Interact to Shape Who We Are (New York: Guilford Press, 1999).
20. This binary decision yields a characteristic “yes” or “no” pattern of cell firing, the neural equivalent of a thumbs up or thumbs down. That neural firing signature lasts for just one-twentieth of a second, holding the decision in place for long enough to give other areas a chance to read it. It takes about ten times longer—around 500 milliseconds—for the yes/no pattern to eventually register distinctly in the OFC. This initial stage of the like/dislike decision takes roughly a half second.
21. If this is a bargaining session—that is, with opportunities for repeated interactions—then the rejection actually becomes rational (and common), as it establishes a bargaining position that pays off in later offers. The rejection is “irrational” only if it occurs in a “one-shot” confidential situation, where there is no opportunity to establish a bargaining position with the cur
rent partner.
22. The more prefrontal activity, the better the outcome of the Ultimatum Game; see Alan G. Sanfey et al., “The Neural Basis of Economic Decision-making in the Ultimatum Game,” Science 300 (2003), pp. 1755–57.
23. The dorsolateral prefrontal area contains an inhibitory array that deploys when we consciously inhibit an impulse. Another route for inhibition travels via the medial area of the prefrontal cortex, which harbors excitatory neurons that activate inhibitory neurons within the amygdala. See Gregory J. Quirk and Donald R. Gehlert, “Inhibition of the Amygdala: Key to Pathological States?” Annals of the New York Academy of Sciences 985 (2003), pp. 263–72. However, neuroscientists disagree about the specifics of pathways for inhibition.
24. On regret, see Natalie Camille et al., “The Involvement of the Orbitofrontal Cortex in the Experience of Regret,” Science 304 (2004), pp. 1167–70.
25. The OFC is but one high-road mechanism for modulating the amygdala. The ventromedial area is another prefrontal region that does so. The influence runs both ways, with the amygdala affecting prefrontal function. Precisely what conditions determine whether the OFC and the amygdala inhibit each other or act synergistically have yet to be discovered.
26. This obliviousness is known as “social anosognia,” the lack of insight into one’s own inappropriateness. For OFC lesion and social gaffes, see Beer et al., “Orbitofrontal Cortex and Social Behavior.”
27. The OFC seems important for regulating behavior implicitly, whereas the dorsolateral prefrontal cortex is important for doing so explicitly. If the latter remains intact, these patients can correct some of their behavior once they become explicitly aware of the fact that they behaved inappropriately. The trick for them is noticing they did something wrong in the first place.
28. On chat rooms, see Kate G. Niederhoffer and James W. Pennebaker, “Linguistic Style Matching in Social Interaction,” Journal of Language and Social Psychology 21 (2002), pp. 337–60.
29. A sign of Internet disinhibition among girls in their early teens is “cyberbullying,” excessively cruel harassment, teasing, and gossip that reduces the target to tears. See Kristin Palpini, “Computer Harassment: Meanness Bottled in a Message,” Daily Hampshire Gazette, December 17, 2005, p. 1. A more ominous downside of cyberdisinhibition is the sleazy practice of adults who via the Internet lure teenagers to perform sex acts in front of webcams in their own homes, in return for payment. See Kurt Eichenwald, “Through His Webcam, a Boy Joins a Sordid Online World,” New York Times, December 19, 2005, p. 1.
30. Kevin Ochsner et al., “Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion,” Journal of Cognitive Neuroscience 14 (2002), pp. 1215–29. The thoughts of the woman are reconstructed from the description of the study.
31. Some MRI studies use special goggles to present the images instead.
32. The dorsolateral prefrontal cortex (PFC) appears to be involved when a person uses language and working memory to work out a new “solution” to an emotional problem, and does so via explicit, deliberative reasoning. By contrast, the OFC regulates emotion apparently via representations of social context, social rules, and so on, which are not explicitly verbalizable. Kevin Ochsner sees this process in terms of associative representations that link actions to affective values. The dorsolateral PFC can hold in mind descriptions of these associations and guide behavior on their basis. See Kevin Ochsner and James Gross, “The Cognitive Control of Emotion,” Trends in Neuroscience 9 (2005), pp. 242–49.
33. On alternate routes, see Kevin Ochsner et al., “For Better or for Worse: Neural Systems Supporting the Cognitive Down- and Up-regulation of Negative Emotion,” NeuroImage 23 (2004), pp. 483–99.
34. Kevin Ochsner, “How Thinking Controls Feeling: A Social Cognitive Neuroscience Approach,” in P. Winkleman and E. Harmon-Jones, eds., Social Neuroscience (New York: Oxford University Press, 2006).
35. On naming an emotion, see A. R. Hariri et al., “Modulating Emotional Response: Effects of a Neocortical Network on the Limbic System,” NeuroReport 8 (2000), pp. 11–43; Matthew D. Lieberman et al., “Putting Feelings into Words: Affect Labeling Disrupts Affect-related Amygdala Activity,” UCLA, unpublished manuscript.
36. Though in the first moment of looping the brain matches our emotions with those we perceive, the high road then offers us a choice point, where we may follow with either of two types of responses. In one we continue to match how the other person feels—their joy gladdens us, their distress upsets us. In the other we feel, for example, envy at their joy or schadenfreude at their distress.
37. On stage fright, see David Guy, “Trying to Speak: A Personal History,” Tricycle (Summer 2003).
38. On the amygdala and social phobia, see, for example, M. B. Stein et al., “Increased Amygdala Activation to Angry and Contemptuous Faces in Generalized Social Phobia,” Archives of General Psychiatry 59 (2002), pp. 1027–34.
39. The lateral portion of the amygdala harbors a site where all sensory information first registers; the nearby central area holds the cells that acquire a fear, according to Joseph LeDoux.
40. For memory reconsolidation, see the work of Karim Nader at McGill University, cited by Joseph LeDoux, presentation at the meeting of the Consortium for Research on Emotional Intelligence in Organizations, Cambridge, Mass., December 14, 2004.
41. This strategy applies both to cognitive therapy and to pharmacological interventions like propranolol. When it comes to overcoming a traumatic fear, reconsolidating the memory with less fear would be neurally direct, according to LeDoux. The neurons that store the fearfulness of the memory are in a part of the amygdala that does not directly connect to the area of the prefrontal cortex that retrieves the conscious aspect of the memory, such as the details of what happened, where, and with whom. But intentional relaxation—as in extinction therapy—utilizes the part of the prefrontal area that links straight to the amygdala’s fear center, offering a route to alter the fearful memory via reconsolidation. LeDoux proposes that each time we reexperience the original fear, we may have a two-hour window for reconsolidation of a fearful memory. Within that window, taking propranolol, which blocks the action of cells in the amygdala (or presumably undergoing deep relaxation as in extinction therapy), alters the reconsolidation so that the amygdala will not react with such fear the next time the traumatic memory is revisited.
42. An alternate theory holds that therapy strengthens prefrontal circuitry that projects to inhibitory circuitry in the amygdala: See Quirk and Gehlert, “Inhibition of Amygdala.”
43. On anger reduction, see Elizabeth Brondolo et al., “Exposure-based Treatment for Anger Problems: Focus on the Feeling,” Cognitive and Behavioral Practice 4 (1997), pp. 75–98. Increasingly, exposure to the stimulus is virtual, as in simulations of an airplane flight.
44. On therapy for social phobia, see David Barlow, Anxiety and Its Disorders (New York: Guilford Press, 1988).
45. LeDoux uses the terms “high” and “low road” here in a particular technical sense, to refer to sensory input pathways to the amygdala from the sensory thalamus and sensory cortex. The “low road” provides a quick and dirty sensory impression, while the high road provides more sensory information. The low road can’t distinguish a snake from a stick, but the high road can. The low road hedges its sensory bets—better safe than sorry. In terms of automatic versus controlled processing—the sense in which I use the high-low road heuristic—LeDoux’s high and low roads are both “low road,” automatic and rapid.
46. The phrase “social brain” was used by noted neuroscientist Michael Gazzaniga in a different sense: not to refer to those parts of the brain active during social interactions, but as a metaphor for the very structure and function of the brain itself. The brain operates like a small society, he argues, whose distinctly independent modules cooperate with one another to perform a given task—much as people agree to work together for a time on some project. However, in the sense I’m using the phrase here, the “social
brain” is the module that orchestrates during person-to-person interactions.
47. Every area of the brain participates in a multitude of functions, so no area is exclusively “social,” save perhaps specialized circuitry like mirror neurons. The fact that an area activates during a given social process does not mean it “causes” that process; involvement is not causation. For more caveats on relating neural activity to social process, see Daniel Willingham and Elizabeth Dunn, “What Neuroimaging and Brain Localization Can Do, Cannot Do, and Should Not Do for Social Psychology,” Journal of Personality and Social Psychology 85 (2003), pp. 662–71.