The Fear Factor

by Abigail Marsh

  “resident nursery companion” at the Cincinnati Zoo: Kelli Bender, “Blakely Plays the Role of Dog Dad to Ohio Zoo’s Rejected Baby Takin,” People, August 18, 2015, http://site.people.com/pets/blakely-plays-the-role-of-dog-dad-to-ohio-zoos-rejected-baby-takin-video/.

  a golden retriever named Izzy: Mike Celizic, “Tigers Say ‘Bye Mom’ to Dog That Raised Them,” Today, June 25, 2009, http://www.today.com/id/31541834/ns/today-today_pets/t/tigers-say-bye-mom-dog-raised-them/#.V-SKiJMrLkI.

  From tiny tamarins and marmosets to siamangs: Karen Isler and Carel P. van Schaik, “Allomaternal Care, Life History, and Brain Size Evolution in Mammals,” Journal of Human Evolution 63, no. 1 (2012): 52–63.

  real allomothering superstars are humans: Hrdy, Mothers and Others.

  Humans in modern cultures: Courtney L. Meehan and Alyssa N. Crittenden, Childhood: Origins, Evolution, and Implications (Albuquerque: University of New Mexico Press, 2016).

  tracing back to the psychiatrist John Bowlby: John Bowlby, A Secure Base: Parent-Child Attachment and Healthy Human Development (New York: Basic Books, 2008); Mary D. Ainsworth, “Infant-Mother Attachment,” American Psychologist 34, no. 10 (1979): 932–937.

  whether child care for working mothers: D’Vera Cohn and Andrea Caumont, “7 Key Findings About Stay-at-Home Moms,” Pew Research Center, April 8, 2014, http://www.pewresearch.org/fact-tank/2014/04/08/7-key-findings-about-stay-at-home-moms/.

  “Children do best in societies”: Quoted in Hrdy, Mothers and Others, 103.

  mothers in some foraging cultures: Ibid., 100.

  Inadequate social support is a top risk factor: Emma Robertson, Sherry Grace, Tamara Wallington, and Donna E. Stewart, “Antenatal Risk Factors for Postpartum Depression: A Synthesis of Recent Literature,” General Hospital Psychiatry 26, no. 4 (2004): 289–295.

  the famous “napalm girl” photograph: Gendy Alimurung, “Nick Ut’s Napalm Girl Helped End the Vietnam War. Today in LA, He’s Still Shooting,” LA Weekly, July 17, 2014, http://www.laweekly.com/news/nick-uts-napalm-girl-helped-end-the-vietnam-war-today-in-la-hes-still-shooting-4861747.

  the awful, heartrending image of Aylan Kurdi: Roy Greenslade, “So Aylan Kurdi’s Picture Did Make a Difference to the Refugee Debate,” The Guardian, September 4, 2015; Jessica Elgot, “Charity Behind Migrant-Rescue Boats Sees 15-Fold Rise in Donations in 24 Hours,” The Guardian, September 3, 2015; Paul Slovic, Daniel Västfjäll, Arvid Erlandsson, and Robin Gregory, “Iconic Photographs and the Ebb and Flow of Empathic Response to Humanitarian Disasters,” Proceedings of the National Academy of Sciences of the United States of America 114, no. 4 (2017): 640–644, DOI: 10.1073/pnas.1613977114.

  what ethologists call “key stimuli”: Leslie A. Zebrowitz, Reading Faces: The Window to the Soul? (Boulder, CO: Westview Press, 1997), 68; Eibl-Eibesfeldt, Love and Hate.

  their brains and the tops of their skulls: Doug Jones, C. Loring Brace, William Jankowiak, Kevin N. Laland, Lisa E. Musselman, Judith H. Langlois, Lori A. Roggman, Daniel Pérusse, Barbara Schweder, and Donald Symons, “Sexual Selection, Physical Attractiveness, and Facial Neoteny: Cross-Cultural Evidence and Implications,” Current Anthropology 36 (1995): 723–748.

  The resulting babyish proportions: Konrad Lorenz, “Die angeborenen Formen moeglicher Erfahrung,” Zeitschrift fur Tierpsychologie 5 (1943): 235–409.

  after adult men and women simply view: Gary D. Sherman, Jonathan Haidt, and James A. Coan, “Viewing Cute Images Increases Behavioral Carefulness,” Emotion 9, no. 2 (2009): 282–286.

  Subjects who were less psychopathic: Jennifer L. Hammer and Abigail A. Marsh, “Why Do Fearful Facial Expressions Elicit Behavioral Approach? Evidence from a Combined Approach-Avoidance Implicit Association Test,” Emotion 15 (2015): 223–231.

  a cute, appealing, babyish appearance: Zebrowitz, Reading Faces.

  These effects are not simply due: Caroline F. Keating, David W. Randall, Timothy Kendrick, and Katharine A. Gutshall, “Do Babyfaced Adults Receive More Help? The (Cross-Cultural) Case of the Lost Résumé,” Journal of Nonverbal Behavior 27, no. 2 (2003): 89–109; David A. Lishner, Luis V. Oceja, E. L. Stocks, and Kirstin Zaspel, “The Effect of Infant-Like Characteristics on Empathic Concern for Adults in Need,” Motivation and Emotion 32 (2008): 270–277.

  Over half of all American households: For a useful summary of academic efforts to explain pet-keeping, with various levels of success, see Melissa Hogenboom, “Why Do We Love Our Pets So Much?” BBC Earth, May 29, 2015, http://www.bbc.com/earth/story/20150530-why-do-we-love-our-pets-so-much.

  one of the causes of rising pet ownership: For articles delving into this possibility, see Robert A. Ferdman, “Modern Family: Americans Are Having Dogs Instead of Babies,” Quartz, April 10, 2014, http://qz.com/197416/americans-are-having-dogs-instead-of-babies/; Karen E. Bender, “Dogs: The Best Kids You Could Ask For,” The Atlantic, August 22, 2014; Jordan Weissmann, “Why America’s Falling Birth Rate Is Sensational News for the Pet Industry,” The Atlantic, May 20, 2013.

  a Russian motorist risked his life: Jenny Starrs, “Harrowing Footage Shows Motorists Dodging Kitten on Busy Russian Highway—Until One Man Stops,” Washington Post, September 16, 2016.

  allomothering provides the basis for altruism: Judith Maria Burkart, O. Allon, Federica Amici, Claudia Fichtel, Christia Finkenwirth, Adolf Heschl, J. Huber, Karin Isler, Z. K. Kosonen, E. Martins, Ellen J. M. Meulman, R. Richiger, K. Rueth, B. Spillmann, S. Wiesendanger, and Carel P. van Schaik, “The Evolutionary Origin of Human Hyper-Cooperation,” Nature Communications 5 (2014): 4747.

  Fearful eyes are wide and large: Roger Segelken, “Survey Explains Why Some Animals Have Smaller Eyes: Lifestyle Matters More Than Size, Cornell Biologists Say,” Cornell Chronicle, August 6, 2004, http://www.news.cornell.edu/stories/2004/08/why-some-animals-have-smaller-eyes-lifestyle-matters.

  adopting a fearful expression causes a face: Abigail A. Marsh, Reginald B. Adams Jr., and Robert E. Kleck, “Why Do Fear and Anger Look the Way They Do? Form and Social Function in Facial Expressions,” Personality and Social Psychology Bulletin 31, no. 1 (2005): 73–86.

  some of our nearest primate relatives: Hillary Anger Elfenbein and Nalini Ambady, “On the Universality and Cultural Specificity of Emotion Recognition: A Meta-Analysis,” Psychological Bulletin 128, no. 2 (2002): 203–235; Signe Preuschoft, “Primate Faces and Facial Expressions.” Social Research 67, no. 1 (2000): 245–271.

  key traits of the one creature that social mammals: Rudolf Schenkel, “Submission: Its Features and Function in the Wolf and Dog,” American Zoologist 7 (1967): 319–329.

  “The plaintive voice of misery”: Adam Smith, The Theory of Moral Sentiments (1853), 48.

  the entry point into the parental care system: Stephanie D. Preston, “The Origins of Altruism in Offspring Care,” Psychological Bulletin 139, no. 6 (2013): 1305–1341.

  regardless of whether the cues: Leslie A. Zebrowitz, Victor X. Luevano, P. Matthew Bronstad, and Itzhak Aharon, “Neural Activation to Babyfaced Men Matches Activation to Babies,” Social Neuroscience 4, no. 1 (2009): 1–10; Chris Baeken, Rudi De Raedt, Nick F. Ramsey, Peter Van Schuerbeek, Dora Hermes, Axel Bossuyt, Lemke Leyman, Marie-Anne Vanderhasselt, Johan De Mey, and Robert Luypaert, “Amygdala Responses to Positively and Negatively Valenced Baby Faces in Healthy Female Volunteers: Influences of Individual Differences in Harm Avoidance,” Brain Research 1296 (2009): 94–103. Note that, in new mothers, amygdala activation may be strongest specifically to images of one’s own baby; see S. Ranote, Rebecca Elliott, Kathryn M. Abel, Rachel Mitchell, John Francis William Deakin, and L. Appleby, “The Neural Basis of Maternal Responsiveness to Infants: An fMRI Study,” Neuroreport 15, no. 11 (2004): 1825–1829.

  listening to them results in more activation: Amygdala responsiveness to cries varies impressively as a function of a number of variables, including gender, parental status, personality, and exactly whose infant is crying, but some level of amygdala responsiveness to infant cries is a constant across nearly every study on the topic
; see Kerstin Sander, Yvonne Frome, and Henning Scheich, “fMRI Activations of Amygdala, Cingulate Cortex, and Auditory Cortex by Infant Laughing and Crying,” Human Brain Mapping 28, no. 10 (2007): 1007–1022; Erich Seifritz, Fabrizio Esposito, John G. Neuhoff, Andreas Lüthi, Henrietta Mustovic, Gerhard Dammann, Ulrich von Bardeleben, Ernst W. Radue, Sossio Cirillo, Gioacchino Tedeschi, and Francesco Di Salle, “Differential Sex-Independent Amygdala Response to Infant Crying and Laughing in Parents Versus Nonparents,” Biological Psychiatry 54, no. 12 (2003): 1367–1375; Isabella Mutschler, Tonio Ball, Ursula Kirmse, Birgit Wieckhorst, Michael Pluess, Markus Klarhöfer, Andrea H. Meyer, Frank H. Wilhelm, and Erich Seifritz, “The Role of the Subgenual Anterior Cingulate Cortex and Amygdala in Environmental Sensitivity to Infant Crying,” PLoS One 11, no. 8 (2016): e0161181.

  differs from oxytocin by only one amino acid: Valery Grinevich, H. Sophie Knobloch-Bollmann, Marina Eliava, Marta Busnelli, and Bice Chini, “Assembling the Puzzle: Pathways of Oxytocin Signaling in the Brain,” Biological Psychiatry 79, no. 3 (2015): 155–164. Incidentally, the limited parental care that sea turtles supply is directly supported by vasotocin. When a mother turtle begins to drag herself up onto the beach in preparation for nesting, the amount of vasotocin produced in her hypothalamus begins to climb. As she begins to dig a hole in the sand with her flippers, it increases still further, then spikes dramatically when the nest nears completion. At the moment she deposits her first egg in the nest, vasotocin levels are 1,500 times greater than when they started rising. Production of vasotocin starts to drop shortly thereafter, remaining just detectable as she covers her nest up with sand. By the time she slips back into the sea, vasotocin production has dwindled away to almost nothing. Does this surge in vasotocin feel like anything to a loggerhead? Does some glimmer of maternal concern pass through her craggy head as she tamps sand over her nest? It is impossible to say, although the fact that sea turtles weep briny tears as they lay their ill-fated eggs has caused some to speculate. See Robert A. Figler, Duncan S. MacKenzie, David W. Owens, Paul Licht, and Max S. Amoss, “Increased Levels of Arginine Vasotocin and Neurophysin During Nesting in Sea Turtles,” General and Comparative Endocrinology 73, no. 2 (1989): 223–232.

  the pituitary releases the oxytocin: C. Sue Carter and Margaret Altemus, “Integrative Functions of Lactational Hormones in Social Behavior and Stress Management,” Annals of the New York Academy of Sciences 807 (1997): 164–74.

  injected oxytocin into female rats’ brains: Cort A. Pedersen, John A. Ascher, Yvonne L. Monroe, and Arthur J. Prange Jr., “Oxytocin Induces Maternal Behavior in Virgin Female Rats,” Science 216, no. 4546 (1982): 648–650.

  Oxytocin has been shown to induce: I should emphasize that any complex behavior involves a complex array of processes within the brain, and maternal care is no different. Given this, the widespread agreement that oxytocin’s effects on subcortical structures like the amygdala are the most essential processes supporting neural care is impressive. For reviews on the effects of oxytocin on maternal behavior, see Keith M. Kendrick, “Neural Control of Maternal Behaviour and Olfactory Recognition of Offspring,” Brain Research Bulletin 44, no. 4 (1997): 383–395; Thomas R. Insel and Lawrence E. Shapiro, “Oxytocin Receptors and Maternal Behavior,” Annals of the New York Academy of Sciences 652 (1992): 122–141; C. Sue Carter, “Neuroendocrine Perspectives on Social Attachment and Love,” Psychoneuroendocrinology 23, no. 8 (1998): 779–818; Gareth Leng, Simone L. Meddle, and Alison J. Douglas, “Oxytocin and the Maternal Brain,” Current Opinion in Pharmacology 8, no. 6 (2008): 731–734.

  the amygdala is a central locus: Oliver J. Bosch and Inga D. Neumann, “Both Oxytocin and Vasopressin Are Mediators of Maternal Care and Aggression in Rodents: From Central Release to Sites of Action,” Hormones and Behavior 61, no. 3 (2012): 293–303; Thomas R. Insel, “The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior,” Neuron 65, no. 6 (2010): 768–779.

  News articles suggested that car dealerships: Stefan Lovgren, “‘Trust’ Hormone’s Smell Helps Us Hand over Cash, Study Says,” National Geographic News, June 1, 2005, http://news.nationalgeographic.com/news/2005/06/0601_050601_trustpotion.html.

  a few squirts of oxytocin up each nostril: Abigail A. Marsh, Henry H. Yu, Daniel S. Pine, Elena K. Gorodetsky, David Goldman, and R. J. R. Blair, “The Influence of Oxytocin Administration on Responses to Infant Faces and Potential Moderation by OXTR Genotype,” Psychopharmacology 224, no. 4 (2012): 469–476.

  several other researchers have since reported: Abigail A. Marsh, Henry H. Yu, Daniel S. Pine, and R. J. Blair, “Oxytocin Improves Specific Recognition of Positive Facial Expressions,” Psychopharmacology (Berl) 209, no. 3 (2010): 225–232; Meytal Fischer-Shofty, Simone G. Shamay-Tsoory, Hagai Harari, and Yechiel Levkovitz, “The Effect of Intranasal Administration of Oxytocin on Fear Recognition,” Neuropsychologia 48, no. 1 (2010): 179–184; Meytal Fischer-Shofty, Simone G. Shamay-Tsoory, and Yechiel Levkovitz, “Characterization of the Effects of Oxytocin on Fear Recognition in Patients with Schizophrenia and in Healthy Controls,” Frontiers in Neuroscience 7 (2013): 127; Alexander Lischke, Christoph Berger, Kristin Prehn, Markus Heinrichs, Sabine C. Herpertz, and Gregor Domes, “Intranasal Oxytocin Enhances Emotion Recognition from Dynamic Facial Expressions and Leaves Eye-Gaze Unaffected,” Psychoneuroendocrinology 37, no. 4 (2012): 475–481.

  the findings reported in a 2016 study: Daniele Viviani, Alexandre Charlet, Erwin van den Burg, Camille Robinet, Nicolas Hurni, Marios Abatis, Fulvio Magara, and Ron Stoop, “Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala,” Science 333, no. 6038 (2011): 104–107.

  Their courage seems to result: Oliver Bosch, Simone L. Meddle, Daniela I. Beiderbeck, Alison J. Douglas, and Inga D. Neumann, “Brain Oxytocin Correlates with Maternal Aggression: Link to Anxiety,” Journal of Neuroscience 25, no. 29 (2005): 6807–6815; Oliver J. Bosch, “Maternal Nurturing Is Dependent on Her Innate Anxiety: The Behavioral Roles of Brain Oxytocin and Vasopressin,” Hormones and Behavior 59, no. 2 (2011): 202–212.

  These neurons may signal other cells: For evidence that the amygdala may mediate what would otherwise be a fearful response to infants, see Alison S. Fleming, Frank Vaccarino, and Carola Luebke, “Amygdaloid Inhibition of Maternal Behavior in the Nulliparous Female Rat,” Physiology and Behavior 25, no. 5 (1980): 731–743. This very recent paper on rats provides strong support for this hypothesis: Elizabeth Rickenbacher, Rosemarie E. Perry, Regina M. Sullivan, and Marta A. Moita. “Freezing Suppression By Oxytocin in Central Amygdala Allows Alternate Defensive Behaviours and Mother-Pup Interactions.” Elife 6 (2017), e24080.

  Dysfunction throughout the amygdala: Mark R. Dadds, Caroline Moul, Avril Cauchi, Carol Dobson-Stone, David J. Hawes, John Brennan, and Richard E. Ebstein, “Methylation of the Oxytocin Receptor Gene and Oxytocin Blood Levels in the Development of Psychopathy,” Development and Psychopathology (2014): 33–40; Mark R. Dadds, Caroline Moul, Avril Cauchi, Carol Dobson-Stone, David J. Hawes, John Brennan, Ruth Urwin, and Richard E. Ebstein, “Polymorphisms in the Oxytocin Receptor Gene Are Associated with the Development of Psychopathy,” Development and Psychopathology (2013): 1–11; Joseph H. Beitchman, Clement C. Zai, Katherine Muir, Laura Berall, Behdin Nowrouzi-Kia, Esther Choi, and James L. Kennedy, “Childhood Aggression, Callous-Unemotional Traits, and Oxytocin Genes,” European Child and Adolescent Psychiatry 21 (2012): 125–132.

  Chapter 7: Can We Be Better?

  Gallup polls of thousands of people: Charities Aid Foundation (CAF), “CAF World Giving Index 2016,” https://www.cafonline.org/about-us/publications/2016-publications/caf-world-giving-index-2016.

  Americans donate hundreds of billions of dollars: Corporation for National & Community Service, “Volunteering and Civic Life in America,” https://www.nationalservice.gov/vcla.

  Americans donate over 13 million units of their blood: AABB, “Blood FAQ,” http://www.aabb.org/tm/Pages/bloodfaq.aspx.


  Thousands more Americans undergo: US Department of Health and Human Services, Health Resources and Services Administration, “General FAQ,” https://bloodcell.transplant.hrsa.gov/about/general_faqs/.

  respondents reported having treated: National Wildlife Rehabilitators Association (NWRA), “Facts About NWRA,” http://www.nwrawildlife.org/?page=Facts.

  international wildlife rehabilitation groups: “International Wildlife Rehabilitators,” http://wildlife.rescueshelter.com/international.

  Per capita, Americans donated: Charity Navigator, “Giving Statistics,” http://www.charitynavigator.org/index.cfm/bay/content.view/cpid/42; Philanthropy Roundtable, “Statistics,” http://www.philanthropyroundtable.org/almanac/statistics/.

  Globally, blood donations are also increasing: World Health Organization (WHO), “Blood Safety and Availability,” July 2016, http://www.who.int/mediacentre/factsheets/fs279/en/.

  over three times as many people received marrow: Figure 1 from Dennis Confer and Pam Robinett, “The US National Marrow Donor Program Role in Unrelated Donor Hematopoietic Cell Transplantation,” Bone Marrow Transplantation 42, suppl. 1 (2008): S3–S5.

  Bureau of Labor Statistics (BLS) estimates: Andy Kiersz, “Volunteering in America Is at Its Lowest Level in at Least a Decade,” Business Insider, February 25, 2014, http://www.businessinsider.com/bls-volunteering-chart-2014-2; BLS, “Volunteering in the United States, 2015,” February 25, 2016, https://www.bls.gov/news.release/volun.nr0.htm.

  the trend may instead reflect forces that affect volunteering: “Americans with No Religious Affiliation,” from Pew Research Center, 2014 Religious Landscape Study, http://static6.businessinsider.com/image/55526680ecad04ac07fbd880-1200-900/godless-millennials.png; Corporation for National & Community Service, “National: Trends and Highlights Overview,” https://www.nationalservice.gov/vcla/national.

  Steven Pinker has provided convincing evidence: Steven Pinker, The Better Angels of Our Natures: Why Violence Has Declined (New York: Viking, 2011).