The evolution of the science of stress began in earnest in the first decades of the twentieth century. Famously, in the 1920s, Harvard’s Walter Cannon—echoing Bernard’s earlier concept of a balanced milieu interieur—suggested arousal shifted an animal’s set of internal steady-state conditions, which he termed homeostasis, away from stable habituated set-points [5]. This disequilibrium, in turn, stimulated catecholamine secretion, specifically adrenaline, thereby powering the ‘fight or flight’ emergency response designed to alleviate the imposed challenge, quell the biological disturbance, and facilitate a return to homeostatic normality [6].

A decade later, Hans Selye, switching attention from the catecholamines of the adrenal medulla to the glucocorticoids of the adrenal cortex, began the body of work destined to revolutionize the field. During his early career, Selye observed that rodents who experienced diverse physiological discomforts displayed surprisingly similar stereotypical responses. Regardless of whether rats were electrically shocked, fatigued, starved, or exposed to temperature extremes, observed maladaptations shared a common non-specific trajectory. In his landmark 1936 letter to Nature, Selye described a triad of symptoms, adrenal enlargement, gastrointestinal ulceration, and atrophy of the thymus, which he claimed were predictably elicited by multiple biological insults [7].

The apparent universality of this pathological triad prompted Selye’s formulation of the general adaptation syndrome (GAS). The GAS encapsulated Selye’s core thesis that all biological challenges were countered in a predictable fashion, progressing through the same sequential phases: first alarm, then resistance, and, if the challenge was overwhelming, resulting in the same end product, exhaustion. Selye deployed an engineering term to describe the animal’s response to such perturbation, redefining stress as the “non-specific response of the body to any demand made upon it”, and stressor as any noxious agent stimulating the GAS response [8].

As the twentieth century entered its final quarter, our understanding of stress and its associated vocabulary—homeostasis, fight or flight, the adrenal master gland, GAS—was shaped by these early pioneers. Although superficially recognizing that we each have individually distinct thresholds, set-points, strengths, and vulnerabilities, Selye envisioned the stress response as a stereotypical species-wide phenomenon. The implicit sub-text was of an assumed conformity to imposed demands, whereby stress-induced adaptive responses were tightly bound around the predictable trajectory of the GAS response.

Impacting the Coaching World

Selye once remarked that he never considered the application of his research to sporting domains [9]. Nevertheless, astute coaches quickly recognized its relevance [9, 10]. Influential early translators of Selye’s work to sporting contexts included innovative Australian swim coach Forbes Carlisle, in 1955, track and fields Fred Wilt in the early 1960s, followed by swimming’s legendary James ‘Doc’ Counsilman in 1968 [9,10,11].

Today, Canon and Selye’s legacies remain enshrined within the science of periodization, as evidenced by the persistent citing of homeostasis and GAS as theoretical platforms upon which contemporary planning theory is founded [12,13,14]. The world’s largest strength and conditioning certification body, the National Strength and Conditioning Association, for example, notes the importance of GAS and homeostatic principles within that organization’s publications, stating: “GAS is one of the foundational theories from which the concept of periodization of training was developed” [15]. Similarly, within the academic literature, the only periodization reviews published in high-ranking peer-reviewed journals to date both cite Canon and Selye, noting, for example, that the biological background of periodized designs exploits homeostatic regulation and stress adaptation as fundamental theories of human adaptation [16, 17].

Confusion and Controversy

In the immediate post-war era, Selye’s teachings dominated academic and popular understanding of the stress phenomenon. Concurrently, however, a more psychology influenced research tradition was beginning to navigate its own evolutionary arc. As the century progressed, and these paths transected, ideological conflicts inevitably emerged [18].

Homeostasis and GAS were both firmly biologically entrenched concepts, an issue Selye acknowledged late in life, noting he had long envisioned stress as “a purely physiological and medical phenomenon” [19]. In contrast, psychologists interpreted the stress response as primarily a cognitive event, emerging directly from “a mismatch between individuals’ perceptions of the demands of the task, and their perceptions of their resources for coping with them” [20].

Central to these debates was the origin of the unidentified signal responsible for initially triggering the alarm response, the so-called first mediator. Selye predicted, and fruitlessly searched for, a biological first mediator. More psychologically oriented researchers, however, argued the first mediator was psycho-emotional in genesis, in essence suggesting that events stimulate a stress response only when appraised as ‘threatening’ [18, 21, 22].

Perhaps most notably, throughout the 1960s and 1970s, John Mason—working within Joseph V. Brady’s ground-breaking inter-disciplinary group at Walter Reed Memorial—demonstrated that the stress response varied substantially as a function of the situation, the individual, and the individual’s history. Mason’s work highlighted, for example, that when the noxious psychological concomitants of physical stress were reduced or removed, the GAS either dissipated or disappeared [18, 23]. Simultaneously, classic Selye-inspired theory was straining to accommodate evidence demonstrating that neither homeostasis nor the stress response was static, but varied dynamically under the influence of life history and oscillating biological rhythms. Conventional theory, as illustration, could not eloquently explain why blood pressure fluctuates markedly throughout the day and often remains elevated long after stressors are removed [24].

As the twentieth century entered its final quarter, the explanatory limitations of Selye’s paradigm were increasingly exposed. Most notably, the portrayal of stress as a predictable biologically mediated phenomenon was undermined by (1) the demonstrable effects of non-physical factors on physiological stress responses, and (2) increasingly convincing evidence that stress responses were not generalized and non-specific, but highly individualized and context specific [25].

Revolution to Evolution

As the unifying explanatory power of Selye’s paradigm eroded, the field fragmented. Into this conceptual vacuum, various theories were proposed, but without achieving widespread acceptance [26]. Such was the state of the field when Sterling and Eyer (1988), embracing multi-disciplinary insights, proposed the concept of allostasis [27]. Allostasis suggests that organisms maintain physiological stability by anticipating ‘needs’ before they arise, and by mobilizing a diverse breadth of neurological, biological, and immunological accommodations to counter these emerging challenges [26, 28, 29]. To facilitate this prediction, multi-source information streams are blended with expectations and prior experiences to estimate the ‘threat’ posed by upcoming challenges. Subsequent to this prediction, multiple preemptive remediating actions, calibrated to that perceived threat, are reflexively launched to protect current and future function, thereby promoting survivability.

Allostasis, accordingly, is not a specific set of tightly controlled homeostatic conditions that must be defended, but a set of collaborative processes that strategically deploy resources to preserve functionality in an unpredictable and dynamically changing environment. Consequently, and in contrast to Selye’s model, allostasis recognizes that the neurobiological imperative is not to seek homeostatic permanency (‘stability through constancy’), but to sensitively pre-empt and respond to emerging challenges by orchestrating multi-level system-wide coordinated compensations (‘stability through change’) [24, 28].

Allostatic Accommodation and Load

When the allostatic state is perturbed, a broad sweep of neurological and biological sub-systems collaboratively co-modulate outputs to accommodate imposed demands. Drastic or persistent allostatic accommodations, however, impose a burden: an allostatic load [29]. When operating efficiently, well-calibrated allostatic accommodations sensitively emerge in response to current and anticipated perturbations. These accommodations facilitate positive adaptation for minimal accruing allostatic load, and enhance resilience to future similar stress exposures. In contrast, when allostatic responses are inadequate, overwhelmed, or persistently activated, then excessive accommodative shifts drive accumulating allostatic load [28,29,30].

Although the burden of accumulated load can be gradually alleviated, the legacies of repetitive cycles of accommodation persist as residual traces of neuro-plastic wear and tear. Inevitably, the progressive accumulation of these plastically embedded residues impose penalties. Accordingly persistent or excessive allostatic accommodation drives accumulating load, thereby escalating wear and tear and eroding resilience to future allostatic impositions. This progressive neurobiological wear and tear ultimately manifests as some blend of psycho-emotional, physiological, neurological, immunological, and/or behavioral impairment [30].

Thus, allostatic theory suggests that, when challenged, the organism does not reflexively mount a biologically mediated GAS response powered via the actions of lone families of chemical messengers—Canon’s catecholamines; Selye’s glucocorticoids—as it strives to regain a notionally optimal set of steady-state conditions. Instead, entangled networks of neural and biological collaborators orchestrate concerted responses, deploying arrays of systemic mediators modulated through densely inter-connected non-linear feedback and feedforward linkages [29,30,31]. Allostasis, accordingly, is the complex set of integrated emotional, physiological, immunological, and psychological processes that intimately collaborate to establish a new set of internal conditions best fitting current circumstances [26]. Through these agile adaptive mechanisms, functional robustness on a macro-scale is preserved by persistent synergistic co-modulation on a micro-scale. A phenomenon previously eloquently described as “the beautiful paradox of seeming constancy, despite continuous change” [32].

The Brain as a Master Gland

Selye envisioned biological stress as largely independent of the brain. Allostasis, in contrast, firmly positions the brain as the master organ responsible for orchestrating all central and peripheral responses to imposed challenges [27, 33]. The rapid evolution of neuroimaging techniques has recently validated this assertion. Importantly, contemporary investigations demonstrate that it is the core emotional regions of the brain—highly evolved sites within the amygdala and basal ganglia—that are the first to register challenge, mediate accommodative responses, and are the first networks to exhibit neuro-plastic wear and tear subsequent to unalleviated load [30, 34].

Collectively, these mid-brain modules function as densely interconnected processing hubs, serving to integrate cognition, descending from higher cortical regions, with sensory information emanating from peripheral and visual centers. Such insights affirm that when a perceived change in circumstances alters sensory input, this change is evaluated by the emotion-processing circuitry (along a continuum ranging from ‘benign to threatening’) and an emotional resonance attached to the event. This emotional evaluation subsequently adjusts circulating levels of neurotransmitters, neuromodulators, neuro-hormones, and neural growth factors. These localized neurochemical changes subsequently customize the cascade of downstream biochemical and hormonal responses mobilized to cope with the anticipated challenge [30, 33, 35]. In essence, emotion calibrates the chemistry of the stress response to perceived context.

Contemporary findings thus illustrate that the long sought-after first mediator is not a biological event, but a change in emotional resonance driven by interpretation of sensory events and/or cognitive circumstances [30]. This emotional evaluation subsequently amplifies or dampens the sensations and perceptions deemed immediately pertinent to survival, thereby modulating behaviors and motivational drives. Crucially, these emotionally induced neurochemical alterations are not directly dictated by the intensities of imposed stimuli, but by the emotional resonance afforded the stress-inducing event [28, 30, 33]. Consequently, even when stressors seem far removed from emotional significance, such as cold exposure or laboratory-induced histamine reactions, biological responses can be readily modulated and healing times dramatically extended or foreshortened, simply by manipulating the emotional context [36,37,38]. From this perspective, the stress response is—at its most fundamentally irreducible level—a system-wide survival-promoting neurobiological preparation to cope with anticipated threat, driven by emotional evaluation.

Specifically, in relation to training planning theory, unquestionably, the mechanical and energetic challenges imposed by physical training are the primary instigators of the sequence of neural and biological events that subsequently drive fitness adaptations. Crucially, however, this contemporary updating of Selye’s stress paradigm reveals that the set of adaptations launched in response to training are strongly and inextricably entwined with, and modulated by, background psycho-emotional influences (see Fig. 1).