Evidence indicates that sleep after learning is critical for the subsequent consolidation of human memory. Whether sleep before learning is equally essential for the initial formation of new memories, however, remains an open question. We report that a single night of sleep deprivation produces a significant deficit in hippocampal activity during episodic memory encoding, resulting in worse subsequent retention. Furthermore, these hippocampal impairments instantiate a different pattern of functional connectivity in basic alertness networks of the brainstem and thalamus. We also find that unique prefrontal regions predict the success of encoding for sleep-deprived individuals relative to those who have slept normally. These results demonstrate that an absence of prior sleep substantially compromises the neural and behavioral capacity for committing new experiences to memory. It therefore appears that sleep before learning is critical in preparing the human brain for next-day memory formation-a worrying finding considering society's increasing erosion of sleep time.
Relational memory, the flexible ability to generalize across existing stores of information, is a fundamental property of human cognition. Little is known, however, about how and when this inferential knowledge emerges. Here, we test the hypothesis that human relational memory develops during offline time periods. Fifty-six participants initially learned five ''premise pairs'' (A>B, B>C, C>D, D>E, and E>F). Unknown to subjects, the pairs contained an embedded hierarchy (A>B>C>D>E>F). Following an offline delay of either 20 min, 12 hr (wake or sleep), or 24 hr, knowledge of the hierarchy was tested by examining inferential judgments for novel ''inference pairs'' (B>D, C>E, and B>E). Despite all groups achieving near-identical premise pair retention after the offline delay (all groups, >85%; the building blocks of the hierarchy), a striking dissociation was evident in the ability to make relational inference judgments: the 20-min group showed no evidence of inferential ability (52%), whereas the 12-and 24-hr groups displayed highly significant relational memory developments (inference ability of both groups, >75%; P < 0.001). Moreover, if the 12-hr period contained sleep, an additional boost to relational memory was seen for the most distant inferential judgment (the B>E pair; sleep ؍ 93%, wake ؍ 69%, P ؍ 0.03). Interestingly, despite this increase in performance, the sleep benefit was not associated with an increase in subjective confidence for these judgments. Together, these findings demonstrate that human relational memory develops during offline time delays. Furthermore, sleep appears to preferentially facilitate this process by enhancing hierarchical memory binding, thereby allowing superior performance for the more distant inferential judgments, a benefit that may operate below the level of conscious awareness.association ͉ inference ͉ learning ͉ offline
Appropriate interpretation of pleasurable, rewarding experiences favors decisions that enhance survival. Conversely, dysfunctional affective brain processing can lead to life-threatening risk behaviors (e.g. addiction) and emotion imbalance (e.g. mood disorders). The state of sleep deprivation continues to be associated with maladaptive emotional regulation, leading to exaggerated neural and behavioral reactivity to negative, aversive experiences. However, such detrimental consequences are paradoxically aligned with the perplexing antidepressant benefit of sleep deprivation, elevating mood in a proportion of patients with major depression. Nevertheless, it remains unknown how sleep loss alters the dynamics of brain and behavioral reactivity to rewarding, positive emotional experiences. Using fMRI, here we demonstrate that sleep deprivation amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasure-evoking stimuli. In addition, this amplified reactivity was associated with enhanced connectivity in early primary visual processing pathways and extended limbic regions, yet with a reduction in coupling with medial- and orbito-frontal regions. These neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group, the extent of which exclusively correlated with activity in mesolimbic regions. Together, these data support a view that sleep deprivation is not only associated with enhanced reactivity towards negative stimuli, but imposes a bi-directional nature of affective imbalance, associated with amplified reward-relevant reactivity towards pleasure-evoking stimuli also. Such findings may offer a neural foundation on which to consider interactions between sleep loss and emotional reactivity in a variety of clinical mood disorders.
The drift-diffusion model (DDM) describes decision making in simple, two-alternative forced choice (2AFC) tasks. It accurately fits response-time distributions and implements an optimal decision procedure for stationary 2AFC tasks: for a given accuracy, no other model achieves faster average response times. The value of a decision threshold applied to accumulated information also determines a speed-accuracy tradeoff (SAT) for the DDM, thereby accounting for a ubiquitous feature of human performance in speeded response tasks. However, little is known about how participants settle on particular tradeoffs. One possibility is that they select SATs that maximize the rate of earned rewards. For the DDM, there exist unique, reward-rate-maximizing values for its threshold and starting point parameters in free response tasks that reward correct responses (Bogacz et al, 2006). These optimal values vary as a function of response-stimulus interval, prior stimulus probability and relative reward magnitude for correct responses. We tested the resulting quantitative predictions regarding response time, accuracy and response bias under these task manipulations and found that grouped data conformed well to the predictions of an optimally parameterized DDM.When an organism extracts signals out of noisy inputs from the environment, it faces a fundamental tradeoff: should it spend more time observing a stimulus to increase certainty about its identity and the appropriate response to it, or should it act more quickly at the cost of greater inaccuracy? Such a tradeoff between speed and accuracy has long been recognized as a ubiquitous feature of human behavior in speeded response tasks (Fitts, 1966;Garrett, 1922;Pachella & Pew, 1968;Schouten & Bekker, 1967;Wickelgren, 1977). Yet the factors that lead to a particular tradeoff are still not well understood.Clues about the nature of speed-accuracy tradeoff (SAT) selection have emerged from theoretical and behavioral research on decision making in simple, two-alternative forced choice (2AFC) tasks, which require participants to choose one or the other alternative on every trial (e.g., Audley & Pike, 1965;Busemeyer & Townsend, 1993;LaBerge, 1962;Laming, 1968;Link, 1975;Link & Heath, 1975;Ratcliff, 1978;Smith & Vickers, 1989;Stone, 1960;Usher & McClelland, 2001;Vickers, 1970). Other clues come from physiological research on the neural mechanisms that may underlie this type of decision making (e.g., Carpenter & Williams, 1995;Gold & Shadlen, 2002;Hanes & Schall, 1996;Ratcliff, Cherian, & Segraves, 2003;Roitman & Shadlen, 2002;Schall, 2001;Shadlen & Newsome, 2001;. In particular, a large body of evidence (e.g., Palmer, Huk, & Shadlen, 2005;Ratcliff & Rouder, 2000;Ratcliff, Thapar, Gomez, & McKoon, 2004;Voss, Rothermund, & Voss, 2004) now strongly suggests that decision making in 2AFC tasks can be accurately described by the drift-diffusion model (DDM) (Ratcliff, 1978), for which the SAT can be controlled by adjusting a single parameter (the decision threshold parameter, described bel...
Both sleep and emotion are known to modulate processes of memory consolidation, yet their interaction is poorly understood. We examined the influence of sleep on consolidation of emotionally arousing and neutral declarative memory. Subjects completed an initial study session involving arousing and neutral pictures, either in the evening or in the morning. Twelve hours later, after sleeping or staying awake, subjects performed a recognition test requiring them to discriminate between these original pictures and novel pictures by responding "remember,""know" (familiar), or "new." Selective sleep effects were observed for consolidation of emotional memory: Recognition accuracy for know judgments of arousing stimuli improved by 42% after sleep relative to wake, and recognition bias for remember judgments of these stimuli increased by 58% after sleep relative to wake (resulting in more conservative responding). These findings hold important implications for understanding of human memory processing, suggesting that the facilitation of memory for emotionally salient information may preferentially develop during sleep.
In this paper we investigate tradeoffs between speed and accuracy that are produced by humans when confronted with a sequence of choices between two alternatives. We assume that the choice process is described by the drift diffusion model, in which the speed-accuracy tradeoff is primarily controlled by the value of the decision threshold. We test the hypothesis that participants choose the decision threshold that maximizes reward rate, defined as an average number of rewards per unit of time. In particular, we test four predictions derived on the basis of this hypothesis in two behavioural experiments. The data from all participants of our experiments provide support only for some of the predictions, and on average the participants are slower and more accurate than predicted by reward rate maximization. However, when we limit our analysis to subgroups of 30-50% of participants who earned the highest overall rewards, all the predictions are satisfied by the data. This suggests that a substantial subset of participants do select decision thresholds that maximize reward rate. We also discuss possible reasons why the remaining participants select thresholds higher than optimal, including the possibility that participants optimize a combination of reward rate and accuracy or that they compensate for the influence of timing uncertainty, or both.
The sleep-deprived brain has principally been characterized by examining dysfunction during cognitive-task performance. However, far less attention has been afforded the possibility that sleep deprivation may be as, if not more, accurately characterized on the basis of abnormal resting-state brain activity. Here we report that one night of sleep deprivation significantly disrupts the canonical signature of task-related deactivation, resulting in a double dissociation within anterior as well as posterior midline regions of the default network. Indeed, deactivation within these regions alone discriminated sleep-deprived from sleep-control subjects with a 93% degree of sensitivity and 92% specificity. In addition, the relative balance of deactivation within these default nodes significantly correlated with the amount of prior sleep in the control group (and not extended time awake in the deprivation group). Therefore, the stability and balance of task-related deactivation in key defaultmode regions may be dependent on prior sleep, such that a lack thereof disrupts this signature pattern of brain activity; findings that may offer explanatory insights into conditions associated with sleep loss at both a clinical as well as societal level.
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