Toward a neurobiological model of human performance under pressure

September 1, 2021
118 (36) e2113777118
Research Article
Monkeys exhibit a paradoxical decrease in performance in high-stakes scenarios
Adam L. Smoulder, Nicholas P. Pavlovsky [...] Steven M. Chase
In the penalty shootout of the 2020 Euro soccer championship, Marcus Rashford—a highly talented English player—approached the ball, took a stutter step, and blasted the ball off the side of the goalpost, missing a relatively easy shot that led to England’s defeat. Paradoxically, when the stakes were highest, he performed far below his abilities. Such diminished performance during high-pressure real-time situations, termed “choking under pressure,” extends well beyond sports. For example, someone might prepare extensively for an important presentation yet deliver it poorly in the moment of truth. Various psychological explanations have been offered for this phenomenon; however, no explanation has been established conclusively (1). In PNAS, Smoulder et al. (2) advance an intriguing nonhuman primate model of performance decrements under pressure, complementing previous investigations in humans.
Smoulder et al. (2) trained three Rhesus monkeys (macaca mulatta) to perform a difficult motor reaching task in which both speed and accuracy were required to obtain a reward (Fig. 1). Rewards were given on a trial-by-trial basis in increments of small, medium, and large, but on rare trials the monkeys were cued that an enormous “jackpot” reward would be showered upon them should they perform successfully. For all animals, performance improved with reward size—except on jackpot trials, when it sharply decreased. This pattern persisted after prolonged exposure to the task. Controls demonstrated the necessity of both magnitude and rarity for eliciting performance decrements. The authors thus concluded that this failure to perform the task on jackpot trials is analogous to choking under pressure in humans.
Fig. 1.
Choking under pressure. (A) In practice, a soccer player scores his penalty kick. However, when in a real game in front of an audience, he misses the shot. (BD) Monkeys performed a challenging motor task [Smoulder et al. (2)]. (B) Experimental setup. (C) Small-, medium-, and high-reward trials each occurred with 31.6% probability; jackpot trials occurred with 5% probability. Ahead of each trial, animals were cued with the size of reward that would be given upon successful completion. (D) Performance improved with reward size from small to large reward but markedly diminished on jackpot trials.
Prevalent theories for this curiously irrational phenomenon propose explicit monitoring and distraction as possible underlying psychological mechanisms. Explicit-monitoring theories suggest that excessive attention paid to the step-by-step execution of an automatic skill interferes with performance under pressure (3, 4). On the other hand, distraction theories suggest that in high-pressure situations, task-relevant and -irrelevant thoughts compete for finite attentional resources, decreasing performance (5, 6). Alternate theories emphasize overarousal and anxiety as central to choking (79), and these factors in turn may also interact with attention-based mechanisms. For example, excessive arousal can impair attention and working memory capacities (10), which may facilitate distraction-based choking under pressure.
Smoulder et al. (2) propose that their kinematic analysis of the monkeys’ movement in the reaching task may favor an explicit-monitoring account over distraction to explain the diminished performance on jackpot trials. In an elegant analysis, the authors decomposed reaching into an initial accelerating phase followed by a decelerating phase, termed “ballistic” and “homing,” respectively. For all three animals, distance covered in the ballistic phase decreased progressively with reward size, while time spent in the homing phase increased progressively with reward size. Smoulder et al. suggest that the shorter ballistic phase and longer homing phase indicate that the animals act more cautiously and become more reliant on sensory feedback as reward size increases, in line with the explicit monitoring theory. Reaching cautiousness results in increasingly shorter ballistic motion, and thus the players need to cover a longer distance with the slower homing phase. The “overcautiousness” exerted in the jackpot trials results in the player’s reaching the target after the allotted time has passed, thus failing a trial they could otherwise succeed in. Alternatively, a distraction explanation is also consistent with the observed kinematics: Increased distraction upon first seeing the jackpot cue may leave less time for motor planning ahead of the trial, forcing the animal to rely more heavily on deliberate movement during the trial.
This ambiguity in the underlying mechanisms that lead to choking under pressure reflects important open questions in the human literature. Attention is central to both explicit-monitoring and distraction theories of choking. Therefore, manipulating attention during performance should help differentiate between these accounts if attention plays a key role in choking. Consistent with the distraction theory, functional connectivity between the dorsolateral prefrontal cortex and motor cortex was negatively correlated with choking propensity in a human functional imaging study (6). Yet, attention-based choking interventions in humans resulted in varying and inconsistent effects on performance under pressure (4, 11, 12). Further complicating matters is the fact that evidence in favor of the explicit monitoring theory may be plausibly interpreted as distraction from other task-relevant features, since monitoring oneself inherently diverts attention from elsewhere. Finally, distraction itself as well as attentional lapses may be a result of overarousal or performance anxiety.
Given these multiple, interacting factors, the ability to model this complex human behavior in primates, as Smoulder et al. (2) demonstrate, offers a valuable springboard for future work to ground choking under pressure in a neurobiological explanation. Smoulder et al.’s innovative experimental paradigm can be expanded upon by combining attentional manipulations with physiological measures, neuronal recording, and perturbation in premotor, reward, punishment, attention, and arousal brain circuits. Neural recording techniques in animal models have the advantage of spatial and temporal resolution not readily accessible in humans. Combined with the ability to investigate how neural computations change under perturbation, and with regard to performance, this approach holds promise for dissecting the mechanisms and circuits causally involved in choking under pressure. Moreover, as specific circuits in the primate brain have been associated with different cognitive functions, targeted recordings in primates might further disambiguate the underlying mechanisms. For example, increased activity in the central executive network, such as the dorsolateral prefrontal cortex, the ventrolateral prefrontal cortex, and the supramarginal gyrus in the lateral parietal cortex might favor explicit-monitoring explanations, whereas decreased activity may favor distraction-based theories (1, 13). To tease apart effects of attention from arousal
In PNAS, Smoulder et al. advance an intriguing nonhuman primate model of performance decrements under pressure, complementing previous investigations in humans.
and anxiety, measurements associated with attention, such as eye tracking for gaze location (14), together with autonomic markers of arousal, such as heart rate and galvanic skin response (15), may provide further insight. Likewise, increased activity in reward and punishment brain areas could support an overarousal basis for choking under pressure, as suggested for midbrain (16) and the ventral striatum (17). A tractable animal model is invaluable for systematically investigating any of these circuit predictions.
Social considerations will also be important for expanding on an animal model of choking under pressure. Social fears are especially significant for choking (9), and many of the high-pressure situations encountered in everyday life involve perceived consequences related to social reputation or status. An ideal animal model of choking under pressure will therefore show susceptibility to social pressure. Rhesus monkeys have a strong hierarchical social structure, making fear of negative social judgment particularly relevant, and future work could therefore consider whether social rank modulates choking under pressure.
Taken together, the experimental framework put forth by Smoulder et al. (2) offers unique opportunities for deeper understanding of the neurobiological mechanisms underlying the choking phenomenon. This would be highly valuable for developing better interventions to help people perform to the best of their abilities even in high-pressure situations—with particular relevance for athletes, performance artists, and individuals who experience social anxiety.

Acknowledgments

K.H. is supported by NIH grant DP2 MH126142-01, the Simons Foundation Autism Research Initiative Bridge to Independence Award, a Brain and Behavior Research Foundation Young Investigator Grant, the Whitehall Foundation, and a Sloan Research Fellowship.

References

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T. G. Lee, S. T. Grafton, Out of control: Diminished prefrontal activity coincides with impaired motor performance due to choking under pressure. Neuroimage 105, 145–155 (2015).
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V. S. Chib, S. Shimojo, J. P. O’Doherty, The effects of incentive framing on performance decrements for large monetary outcomes: Behavioral and neural mechanisms. J. Neurosci. 34, 14833–14844 (2014).

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Proceedings of the National Academy of Sciences
Vol. 118 | No. 36
September 7, 2021
PubMed: 34470823

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Published online: September 1, 2021
Published in issue: September 7, 2021

Acknowledgments

K.H. is supported by NIH grant DP2 MH126142-01, the Simons Foundation Autism Research Initiative Bridge to Independence Award, a Brain and Behavior Research Foundation Young Investigator Grant, the Whitehall Foundation, and a Sloan Research Fellowship.

Notes

See companion article, “Monkeys exhibit a paradoxical decrease in performance in high-stakes scenarios,” https://doi.org/10.1073/pnas.2109643118.

Authors

Affiliations

Abraham Saikley
Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305;
Keren Haroush1 [email protected]
Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305;
Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305;
Bio-X Institute, Stanford University, Stanford, CA 94305

Notes

1
To whom correspondence may be addressed. Email: [email protected].
Author contributions: A.S. and K.H. wrote the paper.

Competing Interests

The authors declare no competing interest.

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Toward a neurobiological model of human performance under pressure
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