This book is an important contribution to the study of movement. Shadmehr and Ahmed propose that humans and other animals move in ways that maximize the rate of net utility acquired over time. Moving with greater vigor to obtain a reward costs more energy but secures the reward sooner. Thus, vigor is a mechanism that helps us navigate tradeoffs between time and energy costs. An individual's degree of vigor in pursuit of a given reward offers a window into how much subjective value the individual places on that reward.

But a compelling ecological theory of movement and vigor must also explain why humans and other animals spend so much time not moving. As it turns out, the relative utility of resting may explain a lot about when and how much we choose to move.

Resting (i.e., abstaining from effortful movement) is not a reward-neutral behavior. Much like a motivation to feed generates feelings of hunger; a motivation to rest generates feelings of fatigue (Hockey, Reference Hockey2013). The motivation to rest appears to track both internal information (e.g., nutritional status and illness) and external information (e.g., ambient light and environmental hazards) (Hubbard, Ruppert, Gropp, & Bourgin, Reference Hubbard, Ruppert, Gropp and Bourgin2013; Lima, Reference Lima2005; Schrock, Snodgrass, & Sugiyama, Reference Schrock, Snodgrass and Sugiyama2019; Spurr, Reference Spurr1983).

When we are at rest, our somatic maintenance systems continue to work – identifying and neutralizing toxins and pathogens, repairing tissue damage, digesting food, and synthesizing proteins for a range of other functions (Snodgrass, Reference Snodgrass, Stinson, Bogin and O'Rourke2012). Resting is a behavior that maximizes the metabolic resources available for somatic maintenance. Energy that would otherwise have been spent on movement can instead be spent on somatic maintenance when we are at rest (Westerterp, Reference Westerterp2017).

Rest also has other benefits. For example, resting in a safe place may, on average, reduce the risk of predation or pathogen exposure (Hart, Reference Hart1990; Lima, Reference Lima2005). Resting is so central to our behavioral repertoires that most humans dedicate at least 6 hours of each 24-hour period to obligate rest, in the form of sleep (Nunn & Samson, Reference Nunn and Samson2018). In addition to extended periods of rest at night, human daytime activities are also interspersed with frequent bouts of resting (Munroe et al., Reference Munroe, Munroe, Michelson, Koel, Bolton and Bolton1983).

An individual who moves forfeits the benefits of rest. A motivational system that optimally regulates movement must account for the opportunity costs of giving up rest. For movement to be worthwhile, its net payoff must outweigh the benefits of resting.

The motivation to rest, or at least to minimize movement, is surprisingly strong (Lieberman, Reference Lieberman2015). The high subjective value of resting, in the absence of a compelling reason to move, is illustrated by the fact that many of us find it difficult to maintain minimum levels of physical activity recommended by medical experts (Guthold, Stevens, Riley, & Bull, Reference Guthold, Stevens, Riley and Bull2018), despite the well-known health benefits and social desirability of being physically active.

Human motivational systems that regulate movement evolved in environments where subsistence required relatively demanding physical work and calorie-dense foods were relatively scarce (Eaton, Konner, & Shostak, Reference Eaton, Konner and Shostak1988; Lieberman, Reference Lieberman2015). The evolutionarily novel energetic conditions of many contemporary environments may lead to patterns of movement regulation that are not optimal for long-term cardiometabolic health (Eaton & Eaton, Reference Eaton and Eaton2003).

The average utility of resting, relative to other behaviors, appears to vary widely across species. For example, a comparative study of time allocation budgets in primates, based on direct behavioral observation of free-living populations, reported that the proportion of observed time spent resting varies from 70.3% in Columbian red howler monkeys to 10.9% in common squirrel monkeys (Pollard & Blumstein, Reference Pollard and Blumstein2008). Differences between primate species in resting time are associated with other key determinants of the energy budget, including brain size, body size, and caloric density of the diet (Schrock, Reference Schrock2020).

Changes in the subjective value of resting can have a profound influence on movement and vigor. For example, humans and other animals typically place a greater subjective value on rest when they are sick compared to when they are healthy (Shattuck & Muehlenbein, Reference Shattuck and Muehlenbein2015). Greater lethargy during sickness has been reported in multiple taxa, including humans (Lasselin et al., Reference Lasselin, Karshikoff, Axelsson, Akerstedt, Benson, Engler and Andreasson2020a), nonhuman primates (Friedman, Reyes, & Coe, Reference Friedman, Reyes and Coe1996), rodents (Engeland, Nielsen, Kavaliers, & Ossenkopp, Reference Engeland, Nielsen, Kavaliers and Ossenkopp2001), birds (Owen-Ashley & Wingfield, Reference Owen-Ashley and Wingfield2007), and amphibians (Llewellyn, Brown, Thompson, & Shine, Reference Llewellyn, Brown, Thompson and Shine2011), suggesting that increased resting when sick is a phylogenetically ancient response. This likely reflects, in part, the high energy costs of activating the immune system to fight infection and repair somatic damage (Horan, Little, Rothwell, & Strijbos, Reference Horan, Little, Rothwell and Strijbos1989; Muehlenbein, Hirschtick, Bonner, & Swartz, Reference Muehlenbein, Hirschtick, Bonner and Swartz2010). During illness, calories that are saved by not moving can instead be used to fund the elevated somatic maintenance costs incurred by immune activation (Schrock et al., Reference Schrock, Snodgrass and Sugiyama2019).

Somatic maintenance costs can be manipulated via administration of lipopolysaccharide (LPS) (Lasselin et al., Reference Lasselin, Schedlowski, Karshikoff, Engler, Lekander and Konsman2020b). LPS is a molecule found on Gram-negative bacteria. Many of our cells have receptors that detect LPS circulating in the blood supply and in other tissues. When these receptors detect LPS, it triggers a calorically costly inflammatory immune response aimed at fighting bacterial infection (Horan et al., Reference Horan, Little, Rothwell and Strijbos1989). This inflammatory immune response triggers the classic features of sickness, including lethargy, social withdrawal, reduced appetite, and increased body temperature (Shattuck & Muehlenbein, Reference Shattuck and Muehlenbein2015). The administration of LPS (without causing actual infection) is a commonly used paradigm to study the behavioral and motivation changes that occur during sickness.

One study found that male zebra finches who were housed alone and treated with LPS (to induce sickness) exhibited greater rates of resting behavior compared to male zebra finches who were housed alone and treated with placebo (Lopes, Adelman, Wingfield, & Bentley, Reference Lopes, Adelman, Wingfield and Bentley2012). This experiment was repeated with males who were housed in a breeding colony. When housed in the breeding colony, LPS treatment did not lead to increased resting behavior. Apparently, the proximity of potential mates and social competitors provided sufficient alternative motivations to outweigh the sickness-induced motivation to rest. A follow-up study found that LPS-treated birds who spent more time resting exhibited better immune function, as indexed by bacterial killing capacity, haptoglobin-like activity, and ability to modulate body temperature (Lopes, Springthorpe, & Bentley, Reference Lopes, Springthorpe and Bentley2014). This study provides an example of how resting can play a role in promoting effective somatic maintenance.

Sickness does not force an individual to rest. Rather, sickness increases the subjective value of rest. When alternative motivations that require movement are sufficiently compelling, sick individuals will still move to satisfy those motivations (Lopes, Reference Lopes2014).

For example, one study induced sickness by administering LPS to mouse dams with litters of dependent pups (Aubert, Goodall, Dantzer, & Gheusi, Reference Aubert, Goodall, Dantzer and Gheusi1997). When ambient temperatures were neutral, sick mouse dams reduced their rate of nest building behaviors compared to dams treated with placebo. When experimenters reduced ambient temperatures to colder levels that represented a danger to the pups, sick dams engaged in nearly as much nest building behavior as healthy dams. This study suggests that the increased danger to pups in cold environments generated an alternative motivation sufficiently compelling to at least partially overcome the increased motivation to rest during sickness.

The growing literature on the behavior of sick humans and other animals suggests that the increased subjective value of resting during acute illness is an adaptive response aimed at prioritizing somatic maintenance (Schrock et al., Reference Schrock, Snodgrass and Sugiyama2019; Shattuck & Muehlenbein, Reference Shattuck and Muehlenbein2015). An alternative hypothesis is that the increased motivation to rest in acutely sick individuals is a pathological byproduct of illness. However, the motivational changes that occur during sickness are mediated by highly organized bidirectional communication circuits between the peripheral immune system and the brain (Maier & Watkins, Reference Maier and Watkins1999; McCusker & Kelley, Reference McCusker and Kelley2013). Such highly organized regulatory systems are unlikely evolve for no reason, much less so if they are a net detriment to survival and reproduction. Furthermore, the broad phylogenetic scope of resting as a response to illness suggests that it has been evolutionarily conserved or that it has evolved independently in different lineages (Lasselin et al., Reference Lasselin, Schedlowski, Karshikoff, Engler, Lekander and Konsman2020b; Schrock et al., Reference Schrock, Snodgrass and Sugiyama2019; Shattuck & Muehlenbein, Reference Shattuck and Muehlenbein2015). It should be noted, however, that lethargic states driven by chronic degenerative disease may often be maladaptive (Myers, Reference Myers2008).

Experiments have demonstrated that sick individuals tend exhibit increased aversion to effort relative to healthy individuals (Vichaya & Dantzer, Reference Vichaya and Dantzer2018). In other words, sick individuals perceive a given level effort to be more costly than do healthy individuals. From the viewpoint of resting, this suggests that sickness increases the utility of resting, which, in turn, increases the value a reward must provide in order to make a given level of effort worthwhile.

There has been relatively little direct research on the relationship between sickness and the degree of vigor in patterns of movement. One exception is a study that experimentally induced sickness via LPS administration in human participants and compared walking speed between sick and healthy individuals (Sundelin et al., Reference Sundelin, Karshikoff, Axelsson, Hoglund, Lekander and Axelsson2015). The study reported that LPS-treated individuals walked slower than placebo-treated individuals and that individuals who watched films of participants walking rated the LPS-treated individuals as less healthy than placebo individuals. Slower walkers were rated as looking less healthy, sadder, and more tired compared to faster walkers.

Safe doses of LPS can be used to experimentally manipulate sickness in humans and other animals (Lasselin et al., Reference Lasselin, Schedlowski, Karshikoff, Engler, Lekander and Konsman2020b). The availability of this experimental paradigm opens a wide range of opportunities for novel studies on sickness and movement, including studies of saccade vigor.

Shadmehr and Ahmed briefly touch on resting in one passage of the book, when they discuss a study of locomotion decisions in starlings (Bautista, Tinbergen, & Kacelnik, Reference Bautista, Tinbergen and Kacelnik2001). The birds were trained to pursue rewards via walking or flying and were allowed to make decisions between walking and flying under varying conditions. The starlings made walk versus fly decisions in a manner that was consistent with maximizing the net rate of energy capture. However, the birds frequently opted not to walk or fly but rested instead. This was viewed as a somewhat puzzling behavior because the net rate of energy capture when resting was always negative. The authors of the starling study surmised that, in some cases, the risk of predation might outweigh the benefits of movement (Bautista et al., Reference Bautista, Tinbergen and Kacelnik2001). I propose that that somatic maintenance and the utility of rest are missing pieces of the puzzle that would help make sense of scenarios where individuals abstain from effortful movement, including the starling example.

The literature discussed in this commentary suggests that somatic maintenance is a key variable that influences an individual's decisions about whether to rest or move. Given the amount of time that humans and other animals spend resting (Munroe et al., Reference Munroe, Munroe, Michelson, Koel, Bolton and Bolton1983; Pollard & Blumstein, Reference Pollard and Blumstein2008), the utility of resting is not a trivial detail. It should be included in ecological models of vigor and movement.

I have endeavored to show that resting holds utility that the utility of resting varies depending on an individual's circumstances, and that changes in the utility of resting can lead to changes in patterns of movement. I use sickness as an example, but sickness is not the only circumstance that changes the utility of resting. Other factors that may influence the relative utility of resting include nutritional status (Spurr, Reference Spurr1983), physical exertion (Pageaux & Lepers, Reference Pageaux and Lepers2016), ambient light (Hubbard et al., Reference Hubbard, Ruppert, Gropp and Bourgin2013), and gestation (Butte & King, Reference Butte and King2005), to name a few. If resting held no utility, we would constantly move through our environments, scooping up any reward we could get our hands on. If we hope to explain variation in movement and vigor, we must account for the utility of resting.