Exertion and Pleasure from an Evolutionary Perspective

Michel Cabanac, PhD

Our knowledge of the world, including ourselves, is filtered twice once by the narrow physical or chemical window of our sense, and again by the biological or cultural programming our brains. Both filters are the result of evolution, that is they have been passed down to us because they proved their worth in our ancestors. Such filtering might therefore affect the way we sense and perceive our own bodies. But, first what do words like sense and perceive mean? Sensation is the irruption into consciousness of any nervous message carried to the brain by an afferent pathway. From it, the brain creates a mental object that has four mental dimensions: Quality, or the kind of stimulus; intensity, or how strong it is; hedonicity, or how useful or noxious it is and duration or how long it lasts. Quality, intensity and duration are positive and multiplicative. Only hedonicity is additive , and it can be positive, negative or nil. Such a definition of sensation is simple and has two advantages: 1. It lumps all the different categories of sensations into one category , whereas classical categorization would list many different sorts of sensation with different attributes.
2. It points to a fundamental unity of sensory input to the central nervous system.

More complex than sensation, perception is the simultaneous entry of several afferent messages including those retrieved from memory into consciousness ( Cabanac,1995 ). This book is about humans. Our species, however, evolved from earlier life forms. And this chapter addresses the origin of conscious creatures, their behavior resulting only from tropisms and reflexes. So when, in phylogeny, did consciousness emerge ? my research team has sought the answer in the evolutionary origin of emotional responses. When we gently handled mammals, birds ( Gallus domesticus [ Cabanac & Aizawa, 2000] ) , and reptiles ( lizard, tortoises [Cabanac &Bernieri, 2000 ]), their body temperature rose, producing an emotional fever. This response was produced in reptiles only through behavioral

means and lacking altogether in amphibians ( Cabanac & Cabanac,2004 ) and fish. Gentle handling also accelerated heart rate , another sign of emotion, in mammals, birds (Cabanac & Aizawa, 2000), tortoise (Cabanac &Bernieri, 2000), and lizards, but not in frogs (Cabanac & Cabanac,2000). Because emotional fever and emotional tachycardia exist in mammals, birds, and reptiles, but not in amphibians, the mental experience of emotion may have emerged in evolutionary lineage between amphibians and reptiles. Just as ancient is hedonicity that is the capacity tobassociate different sensation with pleasant or unpleasant responses. Mammals, birds, and reptiles learn to avoid the flavor of a novel food when digestive illness follows ingestion. Such learning is absent from amphibians ( Paradis & Cabanac, 2004 ). Again, the transition from amphibians to reptiles seems to have been a critical evolutionary threshold. These results are consistent with the hypothesis that specific mental capacities emerged with reptiles. According to Darwinian theory, sensory messages should have become conscious because consciousness had proved useful to the organisms first acquiring it. To be useful, these sensations had to describe the quality, the intensity, and above all the usefulness of environtmental stimuli; therefore, it is likely that they were multidimensional from the outset, as defined earlier. The very persistence of consciousness over such a long time span demonstrates its formidable selective advantage. It provided the first sensorially conscious animals with a decisions making edge by optimizing their behavior and by feeing them from the need for an infinitely complex network of hardwired reflexes. It consciousness has a single phylogenetic origin , it is likely that conscious events all share the same basic four dimensional structure (Cabanac,1996). We may now turn to a specific case: the self optimizing nature of feelings aroused by muscular exertion (Ulmer,1996). All that we have defined in the general case of sensation should also hold true here. SENSATIONS FROM MUSCULAR EXERTION Borg has extensively studied the feeling aroused by muscular excertion and has proposed a scale from 6 to 20 called rating of perceived exertion ( RPE ) ( Borg, 1962,1982 ). The feelings measured by Borgs RPE scale are global perceptions arising from various parts of the

body; they are not broken down into their various inputs. Where, then do they originate? During exertion, nervous messages emerge into consciousness not only from the working muscles, tendons, and joints but also from other loci in the body. MUSCLES AND TENDONS In the working apparatus itself , the muscles and tendons, local conditions are modified by exertion. Conscious message are sent via mechanical (Bloomstrand&EssenGustavsson,1987;Gandevia&McCloskey, 1977 ; Roland, 1975 ), chemical ( Starkie et.al., 1999 ), and temperature signals ( Saltin,Gagge,&Stolwijk,1968 ) in relation to the degree of exertion by the muscles. Sensation of muscular exertion thus originates peripherally ( Sanes & Shadmehr,1995; Wade,2003 ). Muscles temperature is an important signal of fatigue but, unexpectedly , not of heat. Cooling significantly shortens the time to reach fatigue and more than halves the work capacity. This is unexpected because cooler muscles require less effort, make less demand on reserves, and create lower concentrations of waste products and by- products. It is not yet understood why fatigue occurs at a particular point or why local cooling reduces work capacity ( Wade et al, 2000) . HEART AND RESPIRATION Many authors have shown that rates of perceived exertion and fatigue are independent of peripheral stimuli. Perceived exertion correlates most highly with blood pressure and not at all with electromyogram readings ( Kilbom et al, 1983 ). Knibestol and Valbo ( 1980 ) conclude that the signal for perceived exertion is central, not peripheral. For Pandolf 9 1978 ), muscular fatigue is fundamentally based on a central signal : Cardiorespiratory stress. Indeed, dyspnea provides a conscious signal that reliably describes the underlying phsyological state ( Mahler & Horowitz, 1994 ) Although heart rate is critical to perceived exertion, it is not the only factor. Heart rate is significantly raised by sleep deprivation even though perceived exertion remains unchanged ( Martin& Haney, 1982 ). The findings of Jackson and colleagues ( 1981 ) do not support a central control model that links perceived exertion solely to cardiovascular stress.

OTHER INTERNAL INFLUENCES If neither peripheral inputs nor cardiorespiratory signals can explain perceived exertion. Other factors may be involved. An important one seems to be lactacidemia : When subjects inhale air with less oxygen, lactacidemia rises with perceived exertion while endurance falls ( Hogan& Welch, 1984 ). Conversely, intravenous glucose perfusion lowers heart rate and respiratory quotient while lowering perceived exertion ( Tabata& Kawakami, 1991 ). Hyperthermia raises lacttacidemia and in turn logarithmically increases perceived exertion (Berg et al., 1986 ), a result also obtained by Kozlowski and colleagues (1985). Core body temperature is thus a limiting factor that may increase discomfort and limit exertion . Temperature has a real but indirect influence. Hyperthermia does not seewm to affect the activation pattern of the muscles. Rather, the linear correlation among core temperature , electroencephalographic recording (EEG), and perceived exertion indicates that changes in cerebral activity may be associated with hyperthermia-induced fatigue during prolonged exercise in hot environment ( Nybo&Nielsen,2001 ). A rise in ambient temperature increases oxygen consumption foR a constant workload and raises the anaerobic fraction. Thus, heat stress cause some blood flow to be dedicated to the thermolysis rather than to muscles ( Dimri et.al, 1980 ). Finally, as may be expected, the sensation of exertion depends on the type of work performed by the muscle. At the start of exercise, sensation is a function of the muscles resistance to the force and is largely independent of whether the work is static or dynamic ( Cafarelli,1982 ). When the work is extended overtime, the sensation of the exertion is of course a function of duration ; the relationship between workload and work duration is hyperbolic when subjects maintain a steady sensation of exertion ( Cafarelli, Cain&Stevens, 1977 ). Different type of work arouse different sensation and also modify the internal environment differently : for an identical workload, light and prolonged aerobic pedaling or weightlifting modifies ventilator flow, heart rate, and level of lactate, cortisol, insulin and blood glucose less than intense but intermittent work ( VanHelder et.al., 1985 ) CONCLUSION The conscious signal is neither purely muscular nor purely central. It is combination of both ( Lollgen, Graham&Sjogaard, 1980; Robertson, 1982 ). There are sensation of the working

muscles and from the heart, yet perceived exertion is not a single sensation but rather an overall perception, as defined earlier. It is worth nothing that the rating of perceived exertion , that is, a mental signal, measures exercise intensity as least as well as heart rate, that is a Physiologycal Index ( Eston, Davies,& Williams,1987; Ueda & Kurokawa, 1991 ). In numerous experimental studies, the subjects rating of perceived exertion predicted their relative metabolic demand, especially at higher workload ( Noble,1982 ). This mental signal reliably adapts behavior to Phsyological capacity. The Borgs scale of overall perceived exertion effectively describes what is taking place overall in the main of a person exerting effort. Is it possible to push this analysis further? By dissociating hedonicity from overall perception, we may find a tool with which to analyze perception. If the hedonic dimension of perception is what motivates and optimizes behavior this will be especially obvious in the case of muscular exertion and the perceptions it arouses. HEDONICITY OF MUSCULAR EXERTION Humans, unlike animal subjects, can verbally describe their sensations. Human experimentation thus enables us to explore the mental experience of muscular exertion and especially to analyze the hedonic content of the perceptions it arouses. To this end, we recorded human sensation in the chest (variable x ) and the lower limbs ( variable y ) and how human perception combine in subjects simply walking on a treadmill with five slopes (x) and five speeds (y) ( Cabanac, 1985 ). The subjects separately estimated displeasure for chest and leg sensations. Figure 6.1 plots these ratings as isohedonic lines ( left box: displeasure in the lower limbs; middle box: displeasure in the chest; right box: sum of the two ratings). These ratings were then compared with actual behavior in other session when the subjects had to climb 300m ( 328 yd ) on the treadmill at varying speeds and slopes. In these new sessions, when a set speed was imposed, the subject could adjust slope, and vice versa. The dots on figure 6.1 show the actual behavior of one subject. The dots fall along the lines, though not generating them, and were from different sessions. Behavior (dots ) was strikingly adapted to the sum of perceived displeasure in the chest and in the lower limbs. Thus, in the situation explored, chest versus lower limbs, behavior was repeatedly consistent: in the bidimensional sensory situation imposed by the experimenters, the subjects

described maps of bidimensional pleasure in session investigating pleasure and tended to move to areas of minimal displeasure on the maps in sessions investigating behavior. Figure 6.2 compares the behavioral choice ( dots 0 at the end of a session with the theoretical time ( Lines ) needed to climb 300 m ( 328 yd ) as directed, the subject manipulating speed or slope. It can be seen that behavioral choice coincided with the 40 min isochronal curve; that is the subject tended to walk with constant time for a constant work. He exercised at a constant power for the various combinations of slopes and speeds. This makes sense from the standpoint of physiology . the result confirm that perception of muscular exertion (figure 6.1 ) integrates all afferent sensory inputs in addition, behavior is not only motivated by the hedonic dimension of perception, but also optimized through minimization of displeasure ( figure 6.2 ). These conclusions were repeatedly borne out by the findings of other research teams.

When subjects performed a mechanical task, that is, pointing, at a target with their arm in various more or less functional positions, their precision and efficacy were maximal when their posture was most comfortable ( figure 6.3 ). Performance deteriorated with increasing discomfort ( Rossetti, Meckler, & Prablanc, 1994 ). When subjects performed a short ( 10 min )incremental exercise on a electrically stabilized exercise bicycle, their oxygen uptake, leg effort and dyspnea varied significantly with different pedaling frequencies . Oxygen uptake was minimal at 60 rpm and increased at both higher and lower pedaling frequencies. Both leg effort and dyspnea were minimal at 80 rpm; leg effort intensified at higher and lower pedaling frequencies., and dyspnea was most intense at 100 rpm . thus, there was some conflict between minimization of energy expenditure and leg effort at expenditures less than 180 W. leg effort was minimized at the cost of increased energy expenditure ( Chen, Jones, and Killian,1999 ), but the general trend was similar to that of our other experiment. Pleasure aroused by muscular exertion decreased when the intensity of exertion reached maximum aerobic power and bordered on anaerobiosis ( Acevedo et.al., 2003). The same conclusion have also been reached by Ekkekakis, Hall, & Petruzzello ( 2005 ) : when exertion

became anaerobic, formerly pleasurable muscular effort now aroused displeasure. Oxygen consumption tended spontaneously to be minimal when subjects could select their own pace (Zarrugh, Todd, & Ralston,1974); indeed, that was what they did ( Zarrugh& Radcliffe, 1978 ). The same type of of optimization also took place in swimming; the stroke frequency spontaneously selected to achieve nmaximum speed was indeed the optimal one for oxygen consumption ( Swaine& Reilly, 1983 )

When the intensity of treadmill work rose, the perception of activation also rose from 2 to 5 ( scale 1 to 6 )and shifted from agreeable to disagreeable, +3 to -1.5 ( scale -5 to +5 ). The working muscles produced a clearly negative alliesthesia of -2 to -3 points. The same stimulus, that is, muscular exertion , can thus arouse either pleasure or displeasure according to the is interrupted, the general perception becomes immediately circumstances. When exertion

pleasurable. Thus, hedonicity is actually the means whereby the muscular system is optimized

and whereby sentient organisms become aware of challenges to homeostasis ( Hall, Ekkekakis, & Petruzzello, 2002 ). This is the very definition of alliesthesia ( Cabanac, 1971 ) Exercise intensity beyond the point of transition from aerobic to aerobic to anaerobic metabolism is accompanied by an exponential decline in affective valence. This change in affect may be a useful guide in helping exercisers recognize their phase of metabolism and thus more effectively self monitor and self regulate the intensity of their efforts ( Ekkekakis, hall, & Petruzzello,2004 ). Ekkekakis distinguishes five types of hedonic responses to the muscular exertion: 1. Brief episodes of pleasure, even at high intensity 2. Strong interindividual differences when exertion is prolonged 3. Universal clear-cut pleasure when exertion ends 4. Universal clear-cut displeasure when exertion borders on exhaustion 5. Universal clear-cut pleasure when intense exertion is interrupted ( Ekkekakis, 2003 ) When mediated by perceptions of exertion, the pursuit of pleasure optimizes

behavior , as assessed by physiological criteria. Pleasure indexes usefulness. Thus, muscular exercise may be intrinsically motivated; that is, muscular exertion in itself might be rewarding. Some daily walking does improve mood ( Thayer et.al, 2004 ). Muscular exertion might also be rewarding because, though unpleasant, it procures another rewards that offsets the unpleasantness of fatigue, for example, fighting the cold by heating oneself through physical exercise. If hedonicity is indeed the signal for behavior optimization, as shown in figure 6.2 and 6.3, it is worth nothing that constant muscular exertion was governed by thresholds of negative hedonicity. Thus behavior was optimizes by minimizing bidimensional displeasure. Such a result does not change the conclusions: Hedonicity is still the optimizer. Yet one may wonder why our subjects would indulge in unpleasant behavior. The answer is that they were motivated to do so. They hate the pleasure of being useful participants in research and receiving a modest financial compensation. Whatever the

motivations, they were motivated to experience displeasure. The hedonicity of exertion had to compete inside them with other hedonicities. We will now turn to the problem of conflicting motivations. HEDONICITY IN MOTIVATIONAL CONFLICTS An organism must rank its priorities because behavior is a final common path: it is not possible to dine and sleep at the same time. To compare motivations and rank them in order of priority, one needs a common currency ( McFarlan& Sibly, 1975 ). I have proposed elsewhere that pleasure is this common currency ( Cabanac, 1992 ). The perception of pleaure, as measured operationally and quantitatively by behavioral choices ( in the case of animals ) or by ratings of the intensity of pleasure ( in the case of humans ), can serve as such a common currency for various motivations. Decisions would be made simply through maximization of the sum of different hedonic values. Is this true in the case of muscular exertion when fatigue is pitted against other motivation ? THERMAL DISCOMFORT VERSUS FATIGUE The hypothesis was verified in the treadmill versus ambient temperature experiments in which a clear cost was involved, either fatigue or cold discomfort. In these experiments, the subjects were placed in a bidimensional ( x,y ) sensory space and had to make a tract of. The result so that there behavior tended to place them in pleasurable areas of this space. The perception of thermal environment was pitted again that of walking on a treadmill ( Cabanac & LeeBlanc, 1983 ). Thermal comfort ( x ) could be improved at the cost of fatigue ( y ). Dressed in swimsuits and tennis shoes, the subjects walked at 3km/hr ( 1.9 mi/hr ) on a treadmill in a climatic chamber. In an initial series of measurements, the treadmill s slope was varied from 0% to 24%, and this conditions was combined with an ambient temperature ranging from 25oC to 5oC in a 25-node matrix. The subjects separately rated the pleasure or displeasure evoked by ambient temperature and by exercise. Actual ratings of pleasure / displeasure of x and y where obtained an ambient temperatures 5o,10o, 15o,20o and 25oC in combination with 0%,, 6%, 12%, 18%, and 24% slopes. The ratings of x and y were totaled . figure 6.4 give the sum of the two

ratings and isohedonic lines interpolated between the nodes. The figure is a map of pleasure in a bidimensional sensory space ( exertion vs. ambient temperature ). In a second series of measurements, one variable was imposed, either treadmill slope or ambient temperature , and the subject could manipulate the other one. The results are also given on figure 6.4 as dots. The subjects reciprocally adjusted exertion intensity and ambient temperature. When a steep slope was imposed, they selected a low ambient temperature, and when walking on a level slope was imposed, they selected a lukewarm ambient temperature. When the subjects were allowed to adjust treadmill slope, with various ambient temperatures being imposed, they selected steep slopes at low ambient temperature and zero slopes at high ambient temperature. Quite strikingly, the dots showing the finally selected experimental conditions ( in quasi- steady states at the end of 1 hr sessions ) are in the white areas indicating bidimensional pleasure. . operant behavior was guided by a tendency to minimize displeasure ( or maximize pleasure ) in a bidimensional space.

Heat production in working muscles may be estimated be three times the amount of mechanical energy produced by the muscle due to the relatively low rentability of the muscle engine. When the subjects walked on the treadmill , the heat production was

inversely proportional to the ambient temperature. Behavioral heat production was proportional to the need to offset heat loss and was therefore optimal for temperature regulation. Taken separately from verbal reports of pleasure / displeasure , these results are consistent with animal observations ( Krebs& Davies, 1981) or experiments ( Collier& Rovee- Collier, 1981 ). Which show a good fit between animal behavior and physiological need. This has been repeatedly demonstrated and needs no further demonstration. Here, however I have gone beyond simple behavior measurement to compare variations in behavior with variations in sensory pleasure, as judged from ratings obtained in separate sessions. Behavior and pleasure follow the same patterns. Thus, the tendency to maximize sensory pleasure serves the purpose of physiological regulation not only in the perception of exercise but also in motivational conflict,. In both cases, pleasure coincides with a clearly adaptive physiological aim. This strongly suggests that pleasure is the key to optimal behavior and that maximizing pleasure leads to optimal physiological performance. If sensory pleasure is the common currency that mediates competing motivations for behaviors with physiological outcomes. It may also mediate other, purely mental motivations. Pleasure may be felt even when no physiological need is being addressed. This was tested in a conflict between exertion and money. STATIC EXERTION VERSUS MONEY In this experiment, human volunteers, could earn money by simply exposing themselves to unpleasant, painful sensations from isometric contractions in their thighs ( Cabanac, 1986 ). They sat with their backs against a wall and their legs at 90o angles, without any chair or stool for support. The longer they remained and endured the pain, the more money they earned,. In several sessions, the rate of pay was varied. It was found that discomfort or pain, as rated by the subjects, increased linearly as a function of time. The subjects also tolerated more intense pain for a longer time when the monetary reward was higher (Figure 6.5). this finding is consistent with common sense. It can be assumed that the subjects decided to end a session just when the displeasure of the sensation became greater than the pleasure of the anticipated monetary reward. The relation

between reward and duration of tolerated displeasure was logarithmic. The hypothesis may thus cover behavioral motivations other than simple sensory hedonicity. The pursuit of pleasure may involve non physiological motivations.

The hedonic dimension of sensation seems to be common currency that mediates the ranking of priorities. The sensations and perceptions aroused by muscular exertion are among many that may be mediated ( Cabanac, 1986 ) ANIMAL STUDIES This conclusion is supported by several animal experiments in which animals had to work for their reward. The amount of work an animal did for an increasingly infrequent reward was used to measure its rewarding effect. Three groups of rats were trained for this experimental design, the rewards being food pellets containing 1%, 10%. And 95% sucrose. When the food pellets were provided continuously, the 10% sucrose ones

maintained the higher work responses rates. When, however the food pellets were provided less snd less often, performance was consistently concentration ( Cheeta, Brooks, & Willner, 1995 ). When fed a tasty diet, rats tend to ingest more. When quinine, a bitter substance, is added to their food, they tend to ingest less and lose weight. In an experiment in which rats had to work for their food, their body weight was the same as when quinine was added to their food and indirect indication that work was aversive ( Peck, 1978 ). When rats had to run on a treadmill for sweet drinks, drinking was related to speed and, to a lesser degree to distance. Thus, the rats must have been comparing information from their own bodies ( rate of energy expenditure ) with their use of a commodity ( sweet reward ) ( Gannon, Smith, & Tierney, 1986 ). Other experiments pitted reproduction (insemination, lactation, nursing ), with costs energy , against food intake, which was also costly. As the rats had to earn food by working on a treadmill ( Perrigo, 1987 ). These experiments provide convincing , albeit indirect, evidence that animals optimize their behavior through hedonic signals. Is it possible to gain more direct evidence that animals will seek sensory pleasure just for the sake of it and even will be ready to trade off some displeasure of it ? Light work must be pleasant to animals, as experiments show that rats will run indefinitely on a treadmill if it is made available ( Jonsdottir et. Al, 1996 ) even when no special reward is obtainable trough running. It may be, then, that work can be pleasurable in itself. As intensity or duration increases, however, work becomes aversive. When monkeys had to pull a chain for heat in a cold environment, they obviously linked the muscular exertion to the warm reward : The increasing force requirement was met with increasing tolerance for larger air temperature fluctuations and longer interval between responses. Eventually they stopped and just sat and shivered ( Adair & Wright, 1976 ) In the obstruction method use by Warden ( 1931 ), rats could reach a bait at the cost of stepping on an unpleasant electrified meshed floor. In a similar but more natural situation, rats were trained to feed in a nest placed at one end of a 16 m (17.5 yd )zigzag alley ( Cabanac & Johnson , 1983 ). The nest was provided with water and food in excess related to sucrose

of the rats needs. On the day of an experimental session, the nest was heated and tasty food ( Shortcake, peanut butter ) was placed 16 m away, but the environment outside the warm nest was cooled to -15oC, a temperature potentially lethal to rats. The rats run the cold feeder for the palatable bait, not out of necessity ( chow was provided at no cost in the warm nest ) but for the pleasure of ingesting the tasty food. The number of trips was related to the tastiness of the food. When chow was placed in the cold feeder instead of shortcake, the rats went to it once and did not return. The rats were quantitatively comparing the pleasure of eating the food with the displeasure of enduring the cold. Other mammals thus seem to behave as humans do in situations in which conflicting motivations have to be resolved, with a central role for pleasure and hedonicity. If such a mechanism exists in mammals, which we can more easily accept as having consciousness, would it also exist in reptiles? The role of sensory pleasure in decision making was verified in iguanas placed in a motivational conflict. The iguanas had to leave a warm refuge, provided with standard food, to reach a tasty but unnecessary bait ( lettuce ) in a cold environment. They nonetheless ventured out into the cold, trading off the coldness of the outside environment for the tastiness of the bait, but only in mild cold. When ambient temperature was 0oC, they remained under the infrared lamp. Like humans, the iguanas seemed to be minimizing their sensory pleasure; thus, they optimized their behavior ( Balasko & Cabanac, 1998 ).

CONCLUSIONS Information on our physiological status is transmitted via signas to the human mind. These signals are critical to survival and must be analyzed, prioritized, and adjudicated to produce an appropriate behavioral response, such as during muscular exertion. This is the role of hedonicity in sensation and perception : to select a behavioral response that is appropriate to both the organisms needs and its physiological capacities. Pleasure/ displeasure is the optimizer of behavior.

Hedonicity must have been an efficacious solution to the problems of life, as it has been retained by successive reptilian and mammalian lineages down to us.because behavior is a final common path, all motivations, including the autohedonicity of exertion itself, compete to access for it. If a motivation to accomplish a given task is given so high a priority that other hedonic messages are ignored, the resulting overexertion may lead to injury or even death, as with Pheddipides , the famous marathon runner ( Cabanac & Bonniot- Cabanac, 1997 ). In most cases however, the inconvenience of fatigue is simply less than the rewards of work. Work is disliked but done nevertheless for the rewards that flow from it. This was the very point of the verse in Genesis. Conversely, acute and chronic physical activity influence brain function, resulting in changes to brain morphology, neuronal firing rates, cellular metabolism, neurotransmitter concentrations and release, number and sensitivity of receptors and level of gene transcription and protein production ( Hoomissen, 2004 ). In the absence of activity, boredom itselfbecomes hedonic motivation ( Mageau, Green-Demers & Pelletier, 2000 ).