The Hour Between Dog and Wolf
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15 it makes us want to repeat these actions Wittmann, B., Daw, N., Seymour, B., Dolan, R. (2008) Striatal Activity Underlies Novelty-Based Choice in Humans. Neuron 58, 967–973.
16 crave these physical activities Robbins, T.W., Everitt, B.J. (1982) Functional studies of the central catecholamines. International Review of Neurobiology 23, 303–365. Robbins, T.W., Everitt, B.J. (1996) Neurobehavioural mechanisms of reward and motivation. Current Opinion in Neurobiology 6, 228–236.
17 animals prefer to work for food than to receive it passively Denny, M. (1957) Learning Through Stimulus Satiation. Journal of Experimental Psychology 54, 62–64. Carder, B., Berkowitz, K. (1970) Rats’ Preference for Earned in Comparison with Free Food. Science 167, 1273–1274. Salamone, J.D., Cousins, M.S., Bucher, S. (1994) Anhedonia or anergia – effects of haloperidol and nucleus-accumbens dopamine depletion on instrumental response selection in a T-maze cost-benefit procedure. Behavioral Brain Research 65, 221–229.
18 the rapid growth of dopamine-producing cells … changed history Fred H. Previc (2009) The Dopaminergic Mind in Human Evolution and History. Cambridge: Cambridge University Press.
19 spontaneous optimism rather than on a mathematical expectation John Maynard Keynes, The General Theory of Employment, Interest and Money. Ch. 12. See also George A. Akerlof and Robert J. Shiller (2009) Animal Spirits: How Human Psychology Drives the Economy, and Why it Matters for Global Capitalism. Princeton University Press.
20 Rat Park Alexander, B.K., Coambs, R.B., Hadaway, P.F. (1978) The effect of housing and gender on morphine self-administration in rats. Psychopharmacology 58, 175–179.
21 will actually kick their habit Solinas, M., Chauvet, C., Thiriet, N., El Rawas, R., Jaber, M. (2008) Reversal of cocaine addiction by environmental enrichment. Proceedings of the National Academy of Sciences 105, 17145–17150.
22 You feel focused, alert, alive, motivated, anticipatory Robert Sapolsky (2004) Why Zebras Don’t Get Ulcers 3rd ed. New York: Henry Holt. Ch. 16.
23 a profound feeling of satisfaction Gregory Berns (2006) Satisfaction: Sensation Seeking, Novelty, and the Science of Finding True Fulfillment. New York: Henry Holt.
24 state often described by psychologists as flow Mihály Csíkszentmihályi (1990), Flow: The Psychology of Optimal Experience. New York: Harper & Row.
25 systems are activated at the same time Quigley, K., Berntson, G. (1990) Autonomic origins of cardiac responses to nonsignal stimuli in the rat. Behavioral Neuroscience 104, 751–762. Berntson, G., Cacioppo, J., Quigley, K. (1991) Autonomic Determinism: The Modes of Autonomic Control, the Doctrine of Autonomic Space, and the Laws of Autonomic Constraint. Psychological Review 98, 459–487.
26 heart and lungs to full speed Another interpretation of heart slowing is that it is merely one part of a pause, occurring throughout body and brain, before we find out what is required of us and which action should be initiated. Jennings et al. likens the pause to clutching in a car. See Jennings, R., van der Molen, M. (2002) Cardiac timing and the central regulation of action. Psychological Research 66, 337–349.
CHAPTER 6: THE FUEL OF EXUBERANCE
1 dopamine in the nucleus accumbens Schroeder, J., Packard, M. (2000) Role of dopamine receptor subtypes in the acquisition of a testosterone conditioned place preference in rats. Neuroscience Letters 282, 17–20. Frye, C., Rhodes, M., Rosellini, R., Svare, B. (2002) The nucleus accumbens as a site of action for rewarding properties of testosterone and its 5alpha-reduced metabolites. Pharmacology Biochemistry Behavior 74, 119–127.
2 making all rewards … much more thrilling Some of this research is described by Donald Pfaff (1999) in his book Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation. Boston: MIT Press. See as well Fuxjager, M.J., Forbes-Lorman, R.M., Coss, D.J., Auger, C.J., Auger, A.P., Marler, C.A. (2010) Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proceedings of the National Academy of Sciences 107, 12393–12398. Caldu, X., Dreher, J. (2007) Hormonal and genetic influences on processing reward and social information. Annals of the New York Academy of Sciences 1118, 43–73.
3 steroids can be addictive Kashkin, K., Kleber, H. (1989) Hooked on hormones? An anabolic steroid addiction hypothesis. Journal of the American Medical Association 262, 3166–3170.
4 involutional melancholia Danziger, L., Schroeder, H., Unger, A. (1944) Androgen Therapy for Involutional Melancholia. Archives of Neurology and Psychiatry 51, 457–461. Altschule, M., Tillotson, K. (1948) The Use of Testosterone in the Treatment of Depressions. New England Journal of Medicine 239, 1036–1038.
5 in 5,000 generations men will be extinct Bryan Sykes (2003) Adam’s Curse: A Story of Sex, Genetics, and the Extinction of Men. Oxford University Press. See as well Steve Jones (2002) Y: The Descent of Men. London: Little, Brown.
6 like sleeper cells in a spy ring Research into these two periods in a male’s life has led to a particularly elegant model of androgen action known as the organisational-activational model, according to which the sensitivity of an adult male to testosterone circulating in his blood depends on how much of the hormone he was exposed to prenatally. (Phoenix, C., Goy, R., Gerall, A., Young, W. (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369–382.) If a male was exposed to a lot of testosterone then he will have dense receptor fields or more sensitive receptors, and consequently later in life he will respond more powerfully to even small increases in the hormone circulating in his blood. If he was exposed to low levels as a foetus then later in life even large increases in testosterone may have a minimal effect.
7 ‘remember’ previously carried sons Williams, T. et al. (2000) Finger-length ratios and sexual orientation. Nature 404, 455–456.
8 higher levels of testosterone in later-born males Schmaltz, G., Quinn, J.S., Schoech, S.J. (2008) Do group size and laying order influence maternal deposition of testosterone in smooth-billed ani eggs? Hormones and Behavior 53, 82–89. Cariello, M.O., Macedo, R.H., Schwabl, H.G. (2006) Maternal androgens in eggs of communally breeding guira cuckoos (Guira guira). Hormones and Behavior 49, 654–662. There is some evidence for the same mechanism operating in humans. Blanchard, R. (1997) Birth order and sibling sex ratio in homosexual versus heterosexual males and females. Annual Review of Sex Research 8, 27–67.
9 deep-seated fear of stocks Ulrike Malmendier and Stefan Nagel also make this point in ‘Depression Babies: Do Macroeconomic Experiences Affect Risk-taking?’ Quarterly Journal of Economics (2011) 126, 373–416.
10 a peak of 44 in 1999 Robert Shiller (2005) Irrational Exuberance 2nd ed. Princeton University Press.
11 a large number of species Chase, I.D., Bartolomeo, C., Dugatkin, L.A. (1994) Aggressive interactions and inter-contest interval: how long do winners keep winning? Animal Behavior 48, 393–400. Rutte, C., Taborsky, M., Brinkhof, M. (2006) What sets the odds of winning and losing? Trends in Ecology and Evolution 21, 16–21.
12 ‘resource holding potential’ … animal can draw on in an all-out fight Hurd, P. (2006) Resource holding potential, subjective resource value, and game theoretical models of aggressiveness signaling. Journal of Theoretical Biology 241, 639–648.
13 chase off a larger, well-fed animal Neat, F., Huntingford, F., Beveridge, M. (1998) Fighting and assessment in male cichlid fish: the effects of asymmetries in gonadal state and body size. Animal Behavior 55, 883–891.
14 choose fights it can win Hsu, Y., Wolf, L. (2001) The winner and loser effect: what fighting behaviours are influenced? Animal Behavior 61, 777–786.
15 deter subsequent opponents from escalating an encounter Rutte, C., Taborsky, M., Brinkhof, M. (2006) What sets the odds of winning and losing? Trends in Ecology and Evolution 21, 16–21.
16 rise in their testosterone levels Wingfield, J.C., Hegner, R.E., Dufty, A.M., Ball, G.F. (1990) The ‘challenge hypothesis’: theoretical implications for pattern
s of testosterone secretion, mating systems, and breeding strategies. American Nauralist 136, 829–846. Oyegbile, T., Marler, C. (2005) Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Hormones and Behavior 48, 259–267.
17 camouflage breaking Falter, C., Arroyo, M., Davis, G. (2006) Testosterone: Activation or organization of spatial cognition? Biological Psychology 73, 132–140. Hines, M. et al. (2003) Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology 28, 1010–1026. Salminen, E., Portin, R., Koskinen, A., Helenius, H., Nurmi, M. (2004) Associations between serum testosterone fall and cognitive function in prostate cancer patients. Clinical Cancer Research 10, 7575–7582.
18 hormone’s tendency to increase an animal’s persistence Andrew, R., Rogers, L. (1972) Testosterone, search behavior and persistence. Nature 237, 343–346. Archer, J. (1977) Testosterone and persistence in mice. Animal Behavior 25, 479–488.
19 and fearlessness Boissy, A., Bouissou, M. (1994) Effects of androgen treatment on behavioral and physiological responses of heifers to fear-eliciting situations. Hormones and Behavior 28, 66–83.
20 the loser with lower levels Trainor, B.C., Bird, I.M., Marler, C.A. (2004) Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Hormones and Behavior 45, 115–121. Fuxjager, M.J., Oyegbile, T.O., Marler, C.A. (2011) Independent and additive contributions of post-victory testosterone and social experience to the development of the winner effect. Endocrinology 152, 3422–3429.
21 intention of depriving … of the benefits of the winner effect Jennings, D., Carlin, C., Gammell, M. (2009) A winner effect supports third-party intervention behavior during fallow deer, Dama dama, fights. Animal Behavior 77, 343–348. Dugatkin, L. (1998) Breaking up fights between others: a model of intervention behaviour. Proceedings of the Royal Society of London B 265, 433–437.
22 even a depressed, state For examples and references see James M. Dabbs (2000) Heroes, Rogues and Lovers: Testosterone and Behavior. New York: McGraw-Hill. pp.88–89.
23 subject to an illusion Gilovich, T., Vallone, R. and Tversky, A. (1985) The hot hand in basketball: On the misperceptions of random sequences. Cognitive Psychology 17, 295–314.
24 winning contributes to further wins Page, L., Coates, J. (forthcoming) The winner effect in human behaviour: quasi-experimental evidence from tennis players.
25 winner effect in humans? Archer, J. (2006) Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews 30, 319–345. Mazur, A., Booth, A. (1998) Testosterone and dominance in men. Behavioral and Brain Sciences 21, 353–397.
26 documented in a number of sports Booth, A., Shelley, G., Mazur, A., Tharp, G., Kittok, R. (1989) Testosterone, and winning and losing in human competition. Hormones and Behavior 23, 556–571. Gladue, B., Boechler, M., McCaul, K.D. (1989) Hormonal response to competition in human males. Aggressive Behavior 15, 409–422.
27 such as tennis Booth, A., Shelley, G., Mazur, A., Tharp, G., Kittok, R. (1989) Testosterone, and winning and losing in human competition. Hormones and Behavior 23, 556–571.
28 wrestling Elias, M. (1981) Serum cortisol, testosterone, and testosterone-binding globulin responses to competitive fighting in human males. Aggressive Behavior 7, 215–224.
29 ice hockey Carré, J., Putnam, S. (2010) Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35, 475–479.
30 chess Mazur, A., Booth, A., Dabbs, J. (1992) Testosterone and chess competition. Social Psychology 55, 70–77.
31 medical exams Mazur, A., Lamb, T.A. (1980) Testosterone, Status, and Mood in Human Males. Hormones and Behavior 14, 236–246.
32 substrate to winning and losing streaks Mazur, A. (1985) A Biosocial Model of Status in Face-to-Face Primate Groups. Social Forces 64, 377–402.
33 home advantage Neave, N., Wolfson, S. (2003) Testosterone, territoriality, and the ‘home advantage’. Physiology and Behavior 78, 269–275. Carré, J., Muir, C., Belanger, J., Putnam, S. (2005) Pre-competition hormonal and psychological levels of elite hockey players: Relationship to the ‘home advantage’. Physiology and Behavior 89, 392–398.
34 achieve just the right levels of testosterone See for example William J. Kraemer, Alan D. Rogol (eds) (2005) The Encyclopaedia of Sports Medicine. An IOC Medical Commission Publication, The Endocrine System in Sports and Exercise, Vol. 11. Oxford: Wiley-Blackwell. Jack H. Wilmore, David L. Costill (2004) Physiology of Sport and Exercise 3rd ed. Human Kinetics Publishers. Per-Olof Astrand, Kaare Rodahl, Hans A. Dahl, Sigmund B. Stromme (2003) Textbook of Work Physiology 4th ed. Human Kinetics Publishers. Frank W. Dick (2007) Sports Training Principles 5th ed. A. & C. Black Publishers Ltd.
35 winning the upcoming game Carré, J., Putnam, S. (2010) Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35, 475–479.
36 manufacture my own intensity thereafter Tim Adams (2003) On Being John McEnroe. New York: Crown Publishers. p.52.
37 these too can raise testosterone levels Carney, D., Cuddy, A., Yap, A. (2010) Power Posing: Brief Nonverbal Displays Affect Neuroendocrine Levels and Risk Tolerance. Psychological Science 21, 1363–1368.
38 music was a ‘divine dynamite’ Quoted in Walter Cannon (1915) Bodily Changes in Pain, Hunger, Fear and Rage: An Account of Recent Researches into the Function of Emotional Excitement. New York: D. Appleton & Co.
39 in others a matter of months Chase, I.D., Bartolomeo, C., Dugatkin, L.A. (1994) Aggressive interactions and inter-contest interval: how long do winners keep winning? Animal Behavior 48, 393–400.
40 elevated testosterone for several years van Anders, S., Watson, N. (2007) Testosterone levels in women and men who are single, in longdistance relationships, or same-city relationships. Hormones and Behavior 51, 286–291. Mazur, A., Michalek, J. (1998) Marriage, Divorce, and Male Testosterone. Social Forces 77, 315–330.
41 than people living in rural areas Beall, C.M., Worthman, C.M., Stallings, J., Strohl, G.M., Brittenham, G.M., Barragan, M. (1992) Salivary testosterone concentration of Aymara men native to 3600m. Annals of Human Biology 19, 67–78.
42 Ache of Paraguay Bribiescas, Richard (1975) Testosterone Levels among Ache Hunter/Gatherer Men: A Functional Interpretation of Population Variation among Adult Males. Human Nature 7, 163–188. James M. Dabbs (2000) Heroes, Rogues and Lovers: Testosterone and Behavior. New York: McGraw-Hill. p.17.
43 World Cup final between Brazil and Italy Bernhardt, P.C., Dabbs, J., Fielden, J., Lutter, C. (1998) Changes in testosterone levels during vicarious experiences of winning and losing among fans at sporting events. Physiology and Behaviour 65, 59–62.
44 experienced vicariously by observers Oliveira, R.F., Lopes, M., Carneiro, L.A., Canário, A.V. (2001) Watching fights raises fish hormone levels. Nature 409, 475. Wingfield, J.C., Marler, P. (1988) Endocrine basis of communication in reproduction and aggression. In Knobil, E., Neill, J. (eds) The Physiology of Reproduction, Vol. 2. New York: Raven Press. pp. 1647–1677. There is also the possibility that hormones participate in mood contagion. Neumann, R., Strack, F. (2000) ‘Mood Contagion’: The Automatic Transfer of Mood Between Persons. Journal of Personality and Social Psychology 79, 211–223. Totterdell, P. (2000) Catching Moods and Hitting Runs: Mood Linkage and Subjective Performance in Professional Sport Teams. Journal of Applied Psychology 85, 848–859.
45 firm in the City of London Coates, J., Herbert, J. (2008) Endogenous steroids and financial risk-taking on a London trading floor. Proceedings of the National Academy of Sciences 105, 6167–6172.
46 when their morning testosterone levels were low The analysis presented here, as in the PNAS paper, relied on a median split on testosterone levels. The analysis can also be carried out using panel data an
d here too the results are highly significant, with correlation coefficients in the 0.36 to 0.39 range, depending on specific analysis used, and p <0.01. I would like to thank Stan Lazic for assistance with these statistics.
47 ratio of the two Manning, J., Scutt, D., Wilson, D., Lewis-Jones, D. (1998) 2nd to 4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction 13, 3000–3004. Manning, J., Taylor, R. (2001) Second to fourth digit ratio and male ability in sport: Implications for sexual selection in humans. Evolution and Human Behavior 22, 61–69. John T. Manning (2002) Digit Ratio: A Pointer to Fertility, Behavior and Health. Rutgers University Press.
48 2D:4D ratios predicted how long these traders had survived in the business Coates, J.M., Gurnell, M., Rustichini, A. (2009) Second-to-fourth digit ratio predicts success among high-frequency financial traders. Proceedings of the National Academy of Sciences 106, 623–628.
49 exactly what it sounds like Cohen-Bendahana, C., van de Beeka, C., Berenbaum, S. (2005) Prenatal sex hormone effects on child and adult sex-typed behavior: Methods and findings. Neuroscience and Biobehavioral Reviews 29, 353–384.
50 called hox-a and hox-d Manning, J., Scutt, D., Wilson, D., Lewis-Jones, D. (1998) 2nd to 4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction 13, 3000–3004. Paul, S., Kato, B., Cherkas, L., Andrew, T., Spector, T. (2006) Heritability of the second to fourth digit ratio (2d: 4d): A twin study. Twin Research and Human Genetics 9, 215–219. Mortlock, D., Innis, J. (1997) Mutation of HOXA13 in hand-foot-genital syndrome. Nature Genetics 15, 179–180.
51 fingers, toes and penises Kondo, T., Zakany, J., Innis, W., Duboule, D. (1997) Of fingers, toes, and penises. Nature 390, 29.
52 increasing their appetite for risk or their confidence Booth, A., Johnson, D., Granger, D. (1999) Testosterone and men’s health. Journal of Behavioral Medicine 22, 1–19. Apicella, C., Dreber, A., Campbell, B., Graye, P., Hoffman, M., Little, A. (2008) Testosterone and financial risk preferences. Evolution and Human Behavior 29, 384–390. Reavis, R., Overman, W. (2001) Adult sex differences on a decision-making task previously shown to depend on the orbital prefrontal cortex. Behavioral Neuroscience 115, 196–206. Van Honk, J. et al. (2004) Testosterone shifts the balance between sensitivity for punishment and reward in healthy young women. Psychoneuroendocrinology 29, 937–943. Schipper, B. (2011) Sex Hormones and Choice under Risk (forthcoming).