The mesolimbic dopaminergic system (ML-DA) allows adapted interactions with the environment and is therefore of critical significance for the individual's survival. The ML-DA system is implicated in ...reward and emotional functions, and it is perturbed in schizophrenia, addiction, and depression. The ML-DA reward system is not only recruited during wakeful behaviors, it is also active during sleep. Here, we introduce the Reward Activation Model (RAM) for sleep and dreaming, according to which activation of the ML-DA reward system during sleep contributes to memory processes, to the regulation of rapid-eye movement (REM) sleep, and to the generation and motivational content of dreams. In particular, the engagement of ML-DA and associated limbic structures prioritizes information with high emotional or motivational relevance for (re)processing during sleep and dreaming. The RAM provides testable predictions and has clinical implications for our understanding of the pathogenesis of major depression and addiction.
Motivational relevance can prioritize information for memory encoding and consolidation based on reward value. In this review, we pinpoint the possible psychological and neural mechanisms by which ...reward promotes learning, from guiding attention to enhancing memory consolidation. We then discuss how reward value can spill-over from one conditioned stimulus to a non-conditioned stimulus. Such generalization can occur across perceptually similar items or through more complex relations, such as associative or logical inferences. Existing evidence suggests that the neurotransmitter dopamine boosts the formation of declarative memory for rewarded information and may also control the generalization of reward values. In particular, temporally-correlated activity in the hippocampus and in regions of the dopaminergic circuit may mediate value-based decisions and facilitate cross-item integration. Given the importance of generalization in learning, our review points to the need to study not only how reward affects later memory but how learned reward values may generalize to related representations and ultimately alter memory structure.
Recent neuroscientific theories have proposed that emotions experienced in dreams contribute to the resolution of emotional distress and preparation for future affective reactions. We addressed one ...emerging prediction, namely that experiencing fear in dreams is associated with more adapted responses to threatening signals during wakefulness. Using a stepwise approach across two studies, we identified brain regions activated when experiencing fear in dreams and showed that frightening dreams modulated the response of these same regions to threatening stimuli during wakefulness. Specifically, in Study 1, we performed serial awakenings in 18 participants recorded throughout the night with high‐density electroencephalography (EEG) and asked them whether they experienced any fear in their dreams. Insula and midcingulate cortex activity increased for dreams containing fear. In Study 2, we tested 89 participants and found that those reporting higher incidence of fear in their dreams showed reduced emotional arousal and fMRI response to fear‐eliciting stimuli in the insula, amygdala and midcingulate cortex, while awake. Consistent with better emotion regulation processes, the same participants displayed increased medial prefrontal cortex activity. These findings support that emotions in dreams and wakefulness engage similar neural substrates, and substantiate a link between emotional processes occurring during sleep and emotional brain functions during wakefulness.
Rapid interruption of ongoing motor actions is crucial to respond to unexpected and potentially threatening situations. Yet, it remains unclear how motor inhibition interacts with emotional ...processes. Here we used a modified stop-signal task including an emotional component (fearful faces) to investigate whether neural circuits engaged by action suppression are modulated by task-irrelevant threat-related signals. Behavioral performance showed that reaction times were prolonged in the presence of incidental threat information, and this emotional slowing was enhanced when incorrect responses were made following stop signals. However, the speed and efficacy of voluntary inhibition was unaffected by emotion. Brain imaging data revealed that emotional cues during stop trials interacted with activity in limbic regions encompassing the basal amygdala and sublenticular extended amygdala region, as well as with the supplementary motor area (SMA). In addition, successful motor inhibition to threat signals selectively recruited a region in lateral orbitofrontal cortex, distinct from areas in inferior frontal gyrus typically associated with voluntary inhibition. Activity in primary motor cortex was lower when incorrect responses were made on stop signal trials accompanied by a fearful face, relative to neutral, in parallel with the slower response times observed behaviorally. Taken together, our findings suggest that the amygdala may not only promote protective motor reactions in emotionally-significant contexts (such as freezing or defensive behavior) but also influence the execution of ongoing actions by modulating brain circuits involved in motor control, so as to afford quick and adaptive changes in current behavior.
► Emotions may entail changes or suppression of ongoing actions ► Interactions between fear and motor control were tested in a stop-signal task ► Fear modulated motor responses via amygdala, lateral orbitofrontal cortex, and SMA ► 3An interaction between threat and stop signals arose in the sublenticular amygdala
Rewarding events enhance memory encoding via dopaminergic influences on hippocampal plasticity. Phasic dopamine release depends on immediate reward magnitude, but presumably also on tonic dopamine ...levels, which may vary as a function of the average accumulation of reward over time. Using model-based fMRI in combination with a novel associative memory task, we show that immediate reward magnitude exerts a monotonically increasing influence on the nucleus accumbens, ventral tegmental area (VTA), and hippocampal activity during encoding, and enhances memory. By contrast, average reward levels modulate feedback-related responses in the VTA and hippocampus in a non-linear (inverted U-shape) fashion, with similar effects on memory performance. Additionally, the dorsal anterior cingulate cortex (dACC) monotonically tracks average reward levels, while VTA-dACC functional connectivity is non-linearly modulated (inverted U-shape) by average reward. We propose that the dACC computes the net behavioral impact of average reward and relays this information to memory circuitry via the VTA.
Rocking has long been known to promote sleep in infants and, more recently, also in adults, increasing NREM sleep stage N2 and enhancing EEG slow waves and spindles. Nevertheless, whether rocking ...also promotes sleep in other species, and what the underlying mechanisms are, has yet to be explored. In the current study, C57BL/6J mice equipped with EEG and EMG electrodes were rocked laterally during their main sleep period, i.e., the 12-h light phase. We observed that rocking affected sleep in mice with a faster optimal rate than in humans (1.0 versus 0.25 Hz). Specifically, rocking mice at 1.0 Hz increased time spent in NREM sleep through the shortening of wake episodes and accelerated sleep onset. Although rocking did not increase EEG activity in the slow-wave and spindle-frequency ranges in mice, EEG theta activity (6–10 Hz) during active wakefulness shifted toward slower frequencies. To test the hypothesis that the rocking effects are mediated through the vestibular system, we used the otoconia-deficient tilted (tlt) mouse, which cannot encode linear acceleration. Mice homozygous for the tlt mutation were insensitive to rocking at 1.0 Hz, while the sleep and EEG response of their heterozygous and wild-type littermates resembled those of C57BL/6J mice. Our findings demonstrate that rocking also promotes sleep in the mouse and that this effect requires input from functional otolithic organs of the vestibule. Our observations also demonstrate that the maximum linear acceleration applied, and not the rocking rate per se, is key in mediating the effects of rocking on sleep.
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•Rhythmic mechanosensory stimulation (aka rocking) promotes sleep also in the mouse•Linear acceleration applied to the head encodes the rocking stimulus•The rocking effects on sleep are acceleration and time specific•The otolithic organs of the vestibular system mediate the rocking effects on sleep
Kompotis et al. demonstrate for the first time that rocking promotes sleep in a species other than the human: i.e., the mouse. They also provide the first evidence that the vestibular otolithic organs mediate sleep promotion and that this effect depends on the linear acceleration applied, and not on the rocking frequency.
Inappropriate behaviors may result from acquiring maladaptive associations between irrelevant information in the environment and important events, such as reward or punishment. Pre-exposure effects ...are believed to prevent the expression of irrelevant associations. For example, learned irrelevance delays the expression of associations between conditioned (CS) and unconditioned (US) stimuli following their uncorrelated presentation. The neuronal substrates of pre-exposure effects in humans are largely unknown because these effects rapidly attenuate when using traditional pre-exposure paradigms. The latter are therefore incompatible with neuroimaging approaches that require many trial repetitions. Moreover, large methodological differences between animal and human research on pre-exposure effects challenge the presumption of shared neurocognitive substrates, and question the prevalent use of pre-exposure effects in animals to model symptoms of human mental disorders. To overcome these limitations, we combined a novel learned irrelevance task with model-based fMRI. We report the results of a model that describes learned irrelevance as a dynamic process, which evolves across trials and integrates the weighting between two state-action values pertaining to ‘CS-no US’ associations (acquired during pre-exposure) and ‘CS-US’ associations (acquired during subsequent conditioning). This relative weighting correlated i) positively with the learned irrelevance effect observed in the behavioral task, ii) positively with activity in the entorhinal cortex, and iii) negatively with activity in the nucleus accumbens (NAcc). Furthermore, the model updates the relative weighting of the two state-action values via two separate prediction error (PE) signals that allow the dynamic accumulation of evidence for the CS to predict the ‘US’ or a ‘no US’ outcome. One PE signal, designed to increase the relative weight of ‘CS-US’ associations following ‘US’ outcomes, correlated with activity in the NAcc, while another PE signal, designed to increase the relative weight of ‘CS-no US’ associations following ‘no US’ outcomes, correlated with activity in the basolateral amygdala. By extending previous animal observations to humans, the present study provides a novel approach to foster translational research on pre-exposure effects.
•Model-based fMRI reveals the neural correlates of learned irrelevance (LIrr) in humans.•LIrr expression correlates positively with entorhinal cortex activity.•LIrr expression correlates negatively with nucleus accumbens (NAcc) activity.•Prediction error signals regulate LIrr and correlates with amygdala/NAcc activity.•The results indicate neuronal overlap between human and animal LIrr.
The functional properties of resting brain activity are poorly understood, but have generally been related to self-monitoring and introspective processes. Here we investigated how emotionally ...positive and negative information differentially influenced subsequent brain activity at rest. We acquired fMRI data in 15 participants during rest periods following fearful, joyful, and neutral movies. Several brain regions were more active during resting than during movie-watching, including posterior/anterior cingulate cortices (PCC, ACC), bilateral insula and inferior parietal lobules (IPL). Functional connectivity at different frequency bands was also assessed using a wavelet correlation approach and small-world network analysis. Resting activity in ACC and insula as well as their coupling were strongly enhanced by preceding emotions, while coupling between ventral-medial prefrontal cortex and amygdala was selectively reduced. These effects were more pronounced after fearful than joyful movies for higher frequency bands. Moreover, the initial suppression of resting activity in ACC and insula after emotional stimuli was followed by a gradual restoration over time. Emotions did not affect IPL average activity but increased its connectivity with other regions. These findings reveal specific neural circuits recruited during the recovery from emotional arousal and highlight the complex functional dynamics of default mode networks in emotionally salient contexts.
►Transient emotions can modulate the brain activity in subsequent resting state. ►Activity in default network shows progressive recovery after emotional conditions. ►ACC-insula coupling during resting state is enhanced after fearful situations. ►Connectivity of IPL with several regions increases at rest after joyful situations. ►Emotion effect on interregional connectivity is specific for higher frequency band.
Some individuals are better at learning about rewarding situations, whereas others are inclined to avoid punishments (i.e., enhanced approach or avoidance learning, respectively). In reinforcement ...learning, action values are increased when outcomes are better than predicted (positive prediction errors PEs) and decreased for worse than predicted outcomes (negative PEs). Because actions with high and low values are approached and avoided, respectively, individual differences in the neural encoding of PEs may influence the balance between approach-avoidance learning. Recent correlational approaches also indicate that biases in approach-avoidance learning involve hemispheric asymmetries in dopamine function. However, the computational and neural mechanisms underpinning such learning biases remain unknown. Here we assessed hemispheric reward asymmetry in striatal activity in 34 human participants who performed a task involving rewards and punishments. We show that the relative difference in reward response between hemispheres relates to individual biases in approach-avoidance learning. Moreover, using a computational modeling approach, we demonstrate that better encoding of positive (vs negative) PEs in dopaminergic midbrain regions is associated with better approach (vs avoidance) learning, specifically in participants with larger reward responses in the left (vs right) ventral striatum. Thus, individual dispositions or traits may be determined by neural processes acting to constrain learning about specific aspects of the world.
Category and letter fluency tasks have been used to demonstrate psychological and neurological dissociations between semantic and phonological aspects of word retrieval. Some previous neuroimaging ...and lesion studies have suggested that category fluency (semantic-based word retrieval) is mediated primarily by temporal cortex, while letter fluency (letter-based word retrieval) is mediated primarily by frontal cortex. Other studies have suggested that both letter and category fluency are mediated by frontal cortex. We tested these hypotheses using voxel-based lesion symptom mapping (VLSM) in a group of 48 left-hemisphere stroke patients. VLSM maps revealed that category and letter fluency deficits correlate with lesions in temporal and frontal cortices, respectively. Other regions, including parietal cortex, were significantly implicated in both tasks. Our findings are therefore consistent with the hypothesis that temporal cortex subserves word retrieval constrained by semantics, whereas frontal regions are more critical for strategic word retrieval constrained by phonology.
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