Abstract
It has been almost a century since the first paper describing a non-linear relationship between arousal and behavioral performance was published (Yerkes and Dodson 1908). This study, an analysis of the influence of task difficulty and stress on discrimination learning in the dancing mouse, stands apart from all others. The paper was published without statistical analyses (statistics had not yet been conceived) and with sample sizes as small as 2 mice per group (an unacceptably low level of power by modern standards). Despite the limitations of their study, the findings of Yerkes and Dodson were subsequently replicated in cats (Dodson, 1915), rats (Broadhurst, 1957; Telegdy and Cohen 1971) and people (Dickman, 2002; Bregman and McAllister 1982; Anderson, 1994), and became part of the lexicon of the field of psychology as the “Yerkes-Dodson Law” (Young, 1936; Eysenk, 1955). In brief, Yerkes and Dodson found that when mice were given a simple discrimination task their performance improved linearly with increases in arousal. With more difficult tasks, the performance of the mice improved with moderate with increases in arousal, but at the highest levels of arousal their performance was impaired, forming an overall non-linear (inverted-U) shaped relationship between arousal and performance. This task-dependent influence on the shape of arousal-performance curves is illustrated in Figure 1.
Illustration of the linear and non-linear components of the Yerkes-Dodson Law based on task difficulty. Performance in both types of tasks is seen to increase in response to a change from low to moderate levels of arousal. Under conditions of high arousal (or specifically “vigor” (Dickman, 2002)), subjects show a high degree of performance in simple tasks, but are impaired in performance in difficult tasks. In general, “simple tasks” would conform to a training condition which involves focused attention to a highly distinct stimulus. Performance on this type of task routinely produces strong and relatively accurate memories under highly arousing conditions, as typified by phenomena such as “weapon focus” and “flashbulb memories”, as well as enhanced memory for central events occurring in an arousing scene (Christianson, 1992; Conway et al., 1994; Safer et al., 1998; Pickel, 1998). By contrast, more demanding tasks that involve divided attention, working memory, attention to cues outside of the source of arousal, or those that involve subtle differences between stimuli in discrimination tasks would conform to the “difficult task” distinction. High levels of arousal typically impair performance in these types of tasks (Leon and Revelle 1985; Burke et al., 1992; Christianson, 1992). Ultimately, our understanding of the complex relationships among task difficulty, arousal and memory will be substantiated by studying the activation or inhibition of different brain memory systems by different levels of task difficulty and arousal (Barch et al., 1997; Arnsten, 1998; Diamond et al., 2001; Braver et al., 2001; Kensinger et al., 2003; Kensinger and Corkin 2004; Birnbaum et al., 2004).
The Yerkes-Dodson Law has served as a continuous influence on cognitive research, with decades of debate involving both support and criticism of its heuristic value (Broadhurst, 1957; Broadhurst, 1959; Brown, 1965; Deffenbacher, 1982; Christianson, 1992; Baumler, 1994; Teigen, 1994; Watters et al., 1997; Dutton and Carroll 2001; Hanoch and Vitouch 2004). Thus, the original work of Yerkes and Dodson and the “Law” it spawned provided the foundation for decades of research into why behavioral performance can be either enhanced or impaired when subjects are under strong pressure (high arousal).
Current research into non-linearities involving arousal and brain function have been conducted at advanced methodological levels that were unimaginable at the time of the birth of the Yerkes-Dodson Law. Neurobiological research has investigated non-linearities in a broad range of investigations of behavior and brain functioning, including functional MRI analysis of working memory (Callicott et al., 1999), hormone-memory interactions (Gold and Van Buskirk 1975; Introini-Collison et al., 1994; Stefani et al., 1999), synaptic plasticity (Diamond et al., 1992; Kerr et al., 1994), receptor ligand-memory interactions (Conrad et al., 1999; Okuda et al., 2004) and neuroprotection in response to metabolic insults (Bar-Joseph et al., 1994; Kaltschmidt et al., 1999; Abraham et al., 2000). It is in this context that I invited researchers with expertise in the study of non-linear relationships involving brain and arousal to submit manuscripts to the journal. The final product is an outstanding effort, with 7 papers contributed by distinguished researchers from 5 different countries. Their work is presented in two special issues devoted to the theme of non-linear relationships involving brain functioning, arousal and behavioral performance.
The current issue contains three papers from researchers in the laboratories of Dr. Corrado Bucherelli of the University of Florence, in Florence, Italy, Dr. Sonia Lupien of the Douglas Hospital Research Center and McGill University, in Montreal, Canada, and Dr. Cheryl Conrad of Arizona State University, in Tempe, Arizona, USA. The first paper by Drs. Baldi and Bucherelli provides a broad perspective on the neural and endocrine basis of non-linearities between behavioral performance and arousal. These investigators present a synthesis, derived from decades of research on rodents and humans, which enhances our understanding of the complex modulation of memory by arousal. Specifically, they have discussed the non-linear relationship between memory and the actions of hormones of the sympathetic nervous system, e.g., epinephrine, and hypothalamic-pituitary-adrenal (HPA) axis, e.g., adrenocorticotropic hormone (ACTH) and glucocorticoids (GCs; corticosterone in the rat and cortisol in people).
The second and third papers in this issue by Drs. Lupien and Conrad focus primarily on the acute effects of GCs on cognition in rodents and people. Both papers discuss evidence that an intermediate level of glucocorticoids enhance, and high levels of GCs impair, memory-related functioning of the hippocampus, a structure that has long been known to be highly sensitive to stress and to be critically involved in learning and memory (Eichenbaum, 2001; Poldrack and Packard 2003). Each of these papers provides balance in pointing out that elevated levels of stress or glucocorticoids may also enhance attention and memory, depending on whether the information is a part of, or outside of, the stress context, as well as whether the stress occurs at the time of acquisition versus the retrieval phase of memory (see also Roozendaal, 2000 for related discussion). This added level of complexity, i.e., that the shape of the function between GC levels and memory is context-dependent, is consistent with the primary feature of the Yerkes and Dodson Law which states that high levels of stress or arousal may enhance performance under some conditions and impair performance under other conditions (Figure 1). Thus, the expression of the relationship between GCs (as well as other physiological measures) and cognition can be either linear or non-linear, depending on variables such as the level of task difficulty, involvement of hippocampus versus non-hippocampal structures, as well as contextual and temporal variables (Cordero and Sandi 1998; Akirav et al., 2004; Okuda et al., 2004).
The second issue in this series will contain papers from the laboratories of Dr. Julian Thayer, of the National Institute on Aging, in Baltimore, Maryland, USA, Dr. Gal Richter-Levin, of the University of Haifa, in Haifa, Israel, Dr. Paul Luiten, of the University of Groningen, in Groningen, The Netherlands and Dr. David Diamond, of the University of South Florida and Veterans Hospital, in Tampa, Florida, USA. The paper by Dr. Thayer is perhaps the most eclectic work in this volume, providing a novel perspective on non-linear relationships in different neural systems. Specifically, this work integrates findings on non-linearities in inhibitory processes in different brain structures, e.g., prefrontal cortex and amygdala, as well as GABA receptor dynamics and synaptic plasticity, all within the broad framework of the neural control of the heart as a model system of inhibitory control.
The paper by Drs. Akirav and Richter-Levin focuses on interactions between neural structures. It is difficult enough to understand how brain structures, in isolation, are involved in learning and memory. These investigators have taken on the additional challenge to understand how the amygdala interacts with the hippocampus to influence memory processing. The ideas developed in their paper are consistent with the secondary theme in both of the special issues, that the expression of non-linearities in amygdala-hippocampus interactions is, among other factors, context-dependent.
The final two papers describe GC actions on neuron survival and memory. Their area of commonality is that they both demonstrate that very low or very high levels of GCs can produce adverse effects on hippocampal functioning. Specifically, Drs. Abraham, Meerlo and Luiten reviewed a substantial literature demonstrating that GCs play a potent role in both the survival and death of hippocampal neurons. They have shown that GCs can activate mechanisms involved in neurodegeneration, as well as neuroprotection, depending on the concentration of the steroid. The recurring theme of context-dependency of GC actions on the hippocampus is addressed here, as well. These authors point out, for example, that the adverse effects of high levels of GCs on neuronal death can be nullified by environmental manipulations, such as calorie restriction.
The volume concludes with a paper by Drs. Park, Campbell, Woodson, Smith, Fleshner and Diamond. These authors studied spatial memory in rats under conditions in which GC levels were manipulated behaviorally, by exposing the rats to a predator, or pharmacologically, by administering metyrapone, a GC synthesis inhibitor. They found that an intermediate level of GCs correlated with optimal memory, and very low or high GC levels correlated with impaired memory. Once again, the issue of context-dependency was raised because elevated GC levels, alone, were insufficient to impair spatial memory. Spatial memory was impaired only when elevated GC levels occurred in conjunction with a behavioral stress state (see also Woodson et al., 2003; Okuda et al., 2004 for related findings).
In summary, the explicit theme of these two issues is the non-linear relationship between arousal and brain functioning. However, it should be noted that increasing levels of arousal do not necessarily produce non-linear effects on the brain or behavior, despite the fact that this is how the Yerkes-Dodson Law is routinely portrayed in Psychology textbooks (e.g., Rice, 1999). The influence of the difficulty of the task on the shape of the arousal-performance curve was emphasized by Yerkes and Dodson (1908), as well as in later discussion by Dodson (1917) and in an early Psychology textbook (Young, 1936). However, recognition of the dual non-linear/linear feature of the Yerkes-Dodson Law by contemporary workers is only rarely acknowledged. Even scholars in the field of emotion, brain and memory have relegated the linear component to the status of a mere footnote (Christianson, 1992) or they have disregarded it entirely (Loftus, 1980; Metcalfe and Jacobs 1998; Mendl, 1999; Aston-Jones et al., 2000). The papers in these two issues help to meld neurobiology and psychology, within the context of the complete, i.e., original, version of the Yerkes-Dodson Law, by demonstrating that the ultimate shape of arousal-performance dose-response curves (as linear or curvilinear) depends on intervening variables, such as the nature of the task and contextual influences.
In closing I would like to note that all of the papers in these two special issues of the journal were peer-reviewed, and I thank the reviewers for their time, effort and constructive criticisms of preliminary versions of the manuscripts. I would also like to thank Dr. Ed Calabrese, the editor-in-chief and driving force behind the study of non-linear phenomena throughout the animal and plant kingdoms, for inviting me to serve as the guest editor of this volume. I would also like to thank Barbara Callahan for her assistance with the formatting of the manuscripts.