The fourth part in a series about A General Theory of Behaviour. I examine homeostasis, synchronicity and circadian systems in the regulation of arousal, behaviour and sociality.
This is a beautifully engineered system where homeostatic and circadian influences at multiple levels are integrated to permit optimal integration of mediators in the internal milieu and external world.
Silver and LeSauter, 2008, p. 272
WHAT IS ENTRAINMENT?
Flashing fireflies, singing cicadas, parading flamingos, murmurating starlings, marching soldiers, chanting sports fans, and crowd participation at rock concerts – all have something in common. To varying degrees, they have ‘got rhythm’ – a shared, synchronized, irresistible rhythm of entrainment.
Entrainment is manifested by an endogenous rhythm that is synchronized with an external cycle such as the light-dark cycle with the result that both oscillations converge towards the same frequency. Behavioural entrainment involves a dynamic coupling of behaviour and brain activity between two or more individuals, which may include ‘mirroring’  or other forms of coordinated joint action. In this post I examine the contribution of entrainment, rhythm and synchrony to individual and social behaviour.
Entrainment is a biological construct borrowed from classical mechanics. It is alleged that, in 1666, the Dutch scientist Christiaan Huygens noticed that when two pendulum clocks are set on the same flexible surface, they eventually become synchronized. This interesting phenomenon has been observed with many kinds of devices and also in living organisms that exhibit rhythmic behaviour with a periodic oscillation. Two necessary conditions for rhythmic synchronicity to qualify as entrainment are: (i) at least two autonomous oscillating systems must be present; and (ii) the two systems must interact. The first condition, autonomy, differentiates entrainment from resonance, an increase in an object’s natural frequency amplitude following exposure to another object with a similar frequency. The oscillations of a resonating system cease when the influence of the original impulse emitting system is removed while an entrained oscillation continues.
Over hundreds of millions of years in an environment that changes dramatically over every 24-hour cycle, evolution has produced universal rhythms throughout the plant and animal kingdoms such that each organism’s biochemistry, physiology, and behaviour are organized in diurnal cycles. Many circadian rhythms are persistent even in the absence of the normal diurnal cues of night and day or temperature changes, e.g. while living in caves. Such demonstrations are interpreted as reflecting the operation of an internal biological clock or clocks. The circadian clock system serves as a biological ‘alerter’ that lets us know when significant events are due to happen.
Principle V (Entrainment): The internal CLOCK controls physiological and behavioural processes in synchrony with regular changes in the environment.
Figure 1. The circadian clock and disease. Relationships and interactions between the circadian clock and disease may either be direct or indirect via behaviour and/or sleep (for description of arrow numbers see main text). Social schedules exert their influence on physiology mainly via behaviour (arrow S). The regular daily changes in the environment that the clock uses for its synchronisation (entrainment) to the 24-h world are indicated by arrow Z. Reproduced with permission from ‘The Circadian Clock and Human Health’ by Till Roenneberg & Martha Merrow (2016).
The light-dark (LD) cycle is the most reliable of the external signals enabling entrainment and is referred to as a zeitgeber (i.e. time-giver). LD information is perceived by mammals with retinal photoreceptors and conveyed directly to the suprachiasmatic nucleus (SCN) of the hypothalamus, where it entrains oscillators in what is regarded as the master clock of the organism . Other cyclic inputs, such as temperature, noise, social cues, or fixed mealtimes, also can act as entraining and predictive agents, although usually to a less reliable extent than LD.
An entrainable circadian clock is present in the SCN during fetal development and the maternal circadian system coordinates the phase of the fetal clock to environmental lighting conditions. Even before birth, the organism is entrained to the LD cycle.
Having a CLOCK system is advantageous for predicting and preparing for important events. When food is available only for a limited time each day, it has been observed that rats increase their locomotor activity 2 to 4 hours before the onset of food availability . Similar anticipatory behaviour occurs in other mammals, and in birds, accompanied by increases in body temperature, adrenal secretion of corticosterone, gastrointestinal motility, and activity of digestive enzymes.
It has been proposed that a common design principle applies to the CLOCK in all organisms, from bacteria to humans, and that the circadian clock has existed for at least 2.5 billion years. The predictive mechanism in which physiology and behaviour are ‘tuned’ to the timing of external events allows a competitive advantage.
A zeitgeber can entrain or synchronize an organism’s biological rhythms to the 24-hour LD cycle and 12-month seasonal cycle. Normal circadian rhythms depend upon zeitgebers. When zeitgebers are absent, for example, when a person is placed in a cave or a windowless room, an endogenous rhythm with a period close to that of the Earth’s rotation is provided.
The human CLOCK system consists of a ‘master clock’ in the SCN of the hypothalamus and secondary clocks in different bodily organs. The endocrine system regulates the circadian rhythm and sleep/waking cycle by producing regular hormone releases. Melatonin is produced in the pineal gland under the control of the central circadian pacemaker in the SCN. Melatonin production is low in the light of day and high during the dark of night when it induces and supports sleep. Melatonin supplementation can be used for the treatment of winter depression, sleep disorders, and as a therapy for epilepsy.
Precise estimates of the periods of endogenous circadian rhythms of melatonin, core body temperature, and cortisol in healthy individuals show that the period of the human circadian clock averages 24.18 hours. Cell-autonomous clocks consist of a ‘transcription–translation-based auto-regulatory feedback loop’.
The coupling of internal and external changes by entrainment enables the organism to predict environmental changes. In humans, the circadian rhythm of melatonin production by the pineal gland and of core body temperature are good markers of circadian rhythms when collected under constant conditions. These markers are closely associated with the circadian component of the sleep-wake rhythm as well as with the circadian variation in neurobehavioural performance. 
Body temperature reflects predominantly the CLOCK and neurobehavioral functions are affected by a sleep pressure homeostasis which increases with time awake and may contribute to the phase delay through interaction with the circadian clock. Neurobehavioral functions usually show a circadian decline at night as is observed in CBT, but they continue their decline after CBT begins to rise, making the subsequent 2–6 hour period (clock time approximately 0600–1000) a zone of maximum vulnerability to loss of alertness and to performance failure.
Sleep homeostatic pressure is produced by the SLEEP-REF, which is indexed behaviourally by intensified feelings of sleepiness that occur the longer the time we are awake. Sleep pressure automatically increases during wakefulness and declines during sleep and the feeling of sleepiness that it generates enables us to keep our wake-sleep balance in equilibrium. To some degree sleep pressure can be placed under voluntary control. We can force ourselves to remain awake when there is a strong reason to do so. In addition to subjective sleepiness, sleep homeostatic pressure is indicated by electroencephalographic (EEG) slow wave activity (SWA), which is prominent early in sleep but decreases over the course of sleep. We return to sleep homeostasis in a later post.
Millions of years of evolution have equipped living organisms with two versatile systems that are designed to fine-tune tasks of daily living such as eating, drinking, eliminating, mating and sleeping, with the outside environment. By entraining essential activities to environmental zeitgebers, the CLOCK schedules the servicing of daily needs at optimal and non-overlapping times. In parallel, the REF provides corrective responses to the organism’s continuously changing needs including any unexpected challenges that may come over the horizon. These two complementary systems seamlessly regulate the waking-sleeping cycle and integrate the internal milieu with the contingencies of the proximal world. The CLOCK and REF systems successfully moderate levels of alertness enabling behaviour to be controlled and executed in a coordinated and coherent manner. To quote Silver and LeSauter (2009): “This is a beautifully engineered system where homeostatic and circadian influences at multiple levels are integrated to permit optimal integration of mediators in the internal milieu and external world” (p. 272).
AFFECTIVE AND SOCIAL ENTRAINMENT
As if the advantages of the CLOCK and REF were not already enough, they also provide a fringe benefits. The most important is that they are responsible for a lot pure, unadulterated fun. When people share stories, singing, dancing, ceremonies, rituals and rites of passage, they experience special feelings of joy, social cohesion and fulfilment.
Principle VI (Coalescence): Entrainment and synchronicity occur in shared activity to create cooperation, cohesion and social bonding.
Behavioural entrainment and synchronization in movement, vocalization or beat enable people to match their actions in timing and rhythm and it is this synchronized form of matching that seems to be most beneficial to enjoyment. Many types of joint action transition naturally towards synchrony such as smiling, laughing, cheering, dancing, marching, drumming, stamping, clapping, singing and chanting are all aspects of sociality that contain elements of synchonicity and/or rhythm. When Ed Sheeran packs a stadium of fifty thousand fans and invites them to sing along with him, they absolutely love it and come back for more. Other social behaviours carried out on a reciprocal basis such as conversation, reciting, poetry reading, playing musical instruments in a band or orchestra involve similar levels of shared appreciation of timing and rhythm: The universality of synchronised action across time and space suggests an evolutionary advantage. Apart from having fun, synchronised shared action offers the advantage of increased social cohesion. [AP 014].
Synchrony in all of these types of group performance involves sharing of intentionality in the deliberate production of rhythmic joint actions. Reinforcement of synchrony by the building of trust and cooperation flows from the group performance of music, chanting, drumming or dance and cooperative actions are reinforced by increasing levels of synchrony. Indigenous music and dance facilitates synchrony and strengthens cooperative action and social cohesion. Enjoyment of music and dance as performers or observers is universal to human beings. [AP 015].
When individuals participate in musical performances, even only as observers, any form of joint action involves affective entrainment. More seems to be going on here than simply temporal entrainment because there is a strong affective tone.  Group drumming is known to produce endocrinal and immunological responses that indicate relief of stress.
Affective entrainment of rhythm and beat are associated with interpersonal bonding initiated by the pleasure of moving the body to music and keeping in time with others. The affective components of entrainment are associated with temporal synchronization creating a ‘groove’ which carries a sense of affiliation. This shared trance-like enjoyment can lead to ‘manic’ form of appreciation such as occurred with the “Beatle-mania” of the 1960s.
Jackson et al. investigated the effects of synchrony and physiological arousal on cohesion and cooperation in large naturalistic groups. They manipulated the synchronous and physiologically arousing affordances of a group marching task within a sports stadium with large samples of strangers. Participants’ subsequent movement, grouping, and cooperation were observed via a camera hidden in the stadium’s roof. Synchrony and arousal both showed main effects, predicting larger groups, tighter clustering, and more cooperative behaviour. Synchrony and arousal among participants in cultural rituals strengthen social cohesion. [AP 016].
The origins of social-affective entrainment appear in early-life musical and rhythmic interactions between infants and caregivers e.g., rocking of the cradle, rhythmic ‘baby talk’ and singing of lullabies. When individuals exchange information reciprocally about each other’s mental processes, alignments unfold over time and space, creating a special form of social interaction, an intrinsically shared activity. Alignment of words, thoughts, bodily postures and movements are all forms of “social entrainment” that can produce increases in positive affect, social cohesion and bonding. [AP 017].
Social entrainment can be detected at many levels both physical to the mental. Gallotti, Fairhurst and Frith argue that interacting individuals are dynamically coupled. When people participate in cultural events such as concerts, plays and operas, alignment is detected in brain activity of the participants. Socio-affective entrainment involves continuous mutual adaptation, complementarity, reciprocity and a division of labour including leader–follower roles. As we shall see, social forms of entrainment conspire to bond people together. Cultural events such as concerts, plays and operas, there is an alignment both in brain activity and behaviour of the participants. [AP 018].
- An entrained circadian CLOCK, which is universal to living organisms, synchronizes internal physiology and external behavior with the light-dark cycle and other zeitgebers.
- The predictive CLOCK and reactive REF coordinate behaviour and physiology, including continuous modulation of alertness, waking and sleep.
- Socio-affective entrainment synchronizes shared cultural activities and reinforces social cohesion and bonding.
 Mirroring occurs when one member of a couple does the same thing as the other member, at the same time.
 For simplicity’s sake, we will call the ‘internal circadian clock system’ the ‘CLOCK’.
 Entrainment can be understood as a form of classical conditioning.
 Stokkan, K. A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001). Entrainment of the circadian clock in the liver by feeding. Science, 291(5503), 490-493.
 Reppert, S. M., & Schwartz, W. J. (1983). Maternal coordination of the fetal biological clock in utero. Science, 220(4600), 969-971.
 Mistlberger, R. E., & Rechtschaffen, A. (1984). Recovery of anticipatory activity to restricted feeding in rats with ventromedial hypothalamic lesions. Physiology & behavior, 33(2), 227-235.
 A conservation project at Victoria Falls Safari Lodge in Zimbabwe provides meat to vultures every day at 1 o’clock. Dozens of vultures roost nearby for a few hours every day before feeding time.
 Loudon, A. S. (2012). Circadian biology: a 2.5 billion year old clock. Current Biology, 22(14), R570-R571.
 Czeisler, C. A., Duffy, J. F., Shanahan, T. L., Brown, E. N., Mitchell, J. F., Rimmer, D. W., … & Dijk, D. J. (1999). Stability, precision, and near-24-hour period of the human circadian pacemaker. Science, 284(5423), 2177-2181.
 Takahashi, J. S. (2016). Transcriptional architecture of the mammalian circadian clock. Nature Reviews Genetics.
 Cajochen, C., Chellappa, S., & Schmidt, C. (2010). What keeps us awake?—the role of clocks and hourglasses, light, and melatonin. In International review of neurobiology (Vol. 93, pp. 57-90). Academic Press.
 Goel, N., Basner, M., Rao, H., & Dinges, D. F. (2013). Circadian rhythms, sleep deprivation, and human performance. In Progress in molecular biology and translational science (Vol. 119, pp. 155-190). Academic Press.
 Silver, R., & LeSauter, J. (2008). Circadian and homeostatic factors in arousal. Annals of the New York Academy of Sciences, 1129(1), 263-274.
 Reddish et al. (2013) experimentally examined the importance of shared intentionality in reinforcing cooperation from group synchrony.
 Mogan, Fischer and Bulbulia (2017) meta-analyzed 42 studies of synchrony effects on: (1) prosocial behaviour, (2) perceived social bonding, (2) social cognition, and (3) positive affect. Synchronous actions affected all four domains and synchrony in larger groups increased prosocial behaviour and positive affect, but did not influence synchrony effects on perceived social bonding and social cognition. See: Mogan, R., Fischer, R., & Bulbulia, J. A. (2017). To be in synchrony or not? A meta-analysis of synchrony’s effects on behaviour, perception, cognition and affect. Journal of Experimental Social Psychology, 72, 13-20.
 Musical entrainment appears in different species within the animal kingdom, e.g. synchronization to a beat in a sulphur-crested cockatoo (Cacatua galerita eleonora). Schachner, A., Brady, T. F., Pepperberg, I. M., & Hauser, M. D. (2009). Spontaneous motor entrainment to music in multiple vocal mimicking species. Current Biology, 19(10), 831-836).
 Phillips-Silver, J., & Keller, P. (2012). Searching for roots of entrainment and joint action in early musical interactions. Frontiers in human neuroscience, 6, 26.
 Bittman, B. B., Berk, L. S., Felten, D. L., Westengard, J., Simonton, O. C., Pappas, J., & Ninehouser, M. (2001). Composite effects of group drumming music therapy on modulation of neuroendocrine-immune parameters in normal subjects. Alternative therapies in health and medicine, 7(1), 38.
 Janata, P., Tomic, S. T., and Haberman, J. (2012). Sensorimotor coupling in music and the Psychology of the groove. J. Exp. Psychol. Gen. 141, 54–75. This study suggested that perceptions of ‘being in the groove’ depend on a strong underlying beat, feeling a part of the music, and wanting to move with the beat.
 Like the Beatles, the fans of Franz Lisz, the Hungarian pianist, are claimed to have displayed ‘mania’.
 Jackson, J. C., Jong, J., Bilkey, D., Whitehouse, H., Zollmann, S., McNaughton, C., & Halberstadt, J. (2018). Synchrony and Physiological Arousal Increase Cohesion and Cooperation in Large Naturalistic Groups. Scientific reports, 8(1), 127.
 Gallotti, M., Fairhurst, M. T., & Frith, C. D. (2017). Alignment in social interactions. Consciousness and cognition, 48, 253-261.
 Hasson, U., & Frith, C. D. (2016). Mirroring and beyond: coupled dynamics as a generalized framework for modelling social interactions. Phil. Trans. R. Soc. B, 371(1693), 20150366.