Biology subjects

Payne, J. D.

Publications and source records attributed to Payne, J. D..

5 recordsLinked to original sources

bioRxiv2023

Targeted memory reactivation during non-rapid eye movement sleep enhances neutral, but not negative, components of memory

Emotionally salient components of memory are preferentially remembered at the expense of accompanying neutral information. This emotional memory trade-off is enhanced over time, and possibly sleep, though a process of memory consolidation. Sleep is believed to benefit memory through a process of reactivation during non-rapid eye movement sleep (NREM). Here, targeted memory reactivation (TMR) was used to manipulate the reactivation of negative and neutral memories during NREM sleep. Thirty-one male and female participants encoded scenes containing either a negative or neutral object superimposed on an always neutral background. During NREM sleep, sounds associated with these scenes were replayed, and memory for scene components was tested the following morning. We found that TMR during NREM sleep improved memory for neutral, but not negative scene objects. This effect was associated with sleep spindle activity, with a larger spindle response following TMR cues predicting TMR effectiveness for neutral items only. These findings therefore do not suggest a role of NREM memory reactivation in enhancing the emotional memory trade-off across a 12-hour period but do align with growing evidence of spindle-mediated memory reactivation in service of neutral declarative memory. Significance statementMemory reactivation during sleep is believed to be a key mechanism facilitating consolidation, the strengthening and stabilisation of memories over time. Emotional memories appear to be preferentially consolidated compared to neutral information, but the role sleep-related memory reactivation in this process is still unclear. Here, we found that experimentally reactivating memories during sleep in humans did not preferentially enhance emotional memory components but did improve neutral memory when tested after one night of sleep. These findings speak against a role of memory reactivation in the early stages of memory consolidation.

neuroscience↗

bioRxiv2021

Investigation of the Stress and Sleep Physiology Correlates of Next-Day Memory for Details of a Social Stressor Testing Environment

Despite evidence which demonstrates that psychosocial stress interacts with sleep to modulate memory, research that has examined next-day memory for the stressful environment itself has not accounted for post-stressor sleep. Here, participants completed the Trier Social Stress Test or a matched control task with psychophysiological monitoring and stress hormone assays. After a 24-hour delay that included overnight polysomnographically-recorded sleep, memory for objects in the testing room was assessed by having participants draw the testing room from the previous day from memory. As expected, stressed participants mounted greater psychophysiological and stress hormone responses to the stressor than participants in the control condition. However, there was only weak evidence that stress reactivity and post-encoding sleep interacted to modulate memory for testing room details. Instead, NREM sleep physiology on the night following testing room encoding was positively associated with memory for testing room details, though this association occurred in the control, but not stressed, participants.

neuroscience↗

bioRxiv2020

Medial prefrontal cortex has a causal role in selectively enhanced consolidation of emotional memories after a 24-hour delay: An iTBS study

Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared to co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short (30-minute) and a long delay (24-hour, including a night of sleep) to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information. Significance StatementUnderstanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation (repetitive transcranial magnetic stimulation, rTMS) to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24-hr delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this "tag-and-capture" mechanism during the initial formation of such memories.

neuroscience↗

bioRxiv2020

Slow oscillation-spindle coupling impairs emotional memory consolidation following stress

Both stress and sleep enhance emotional memory. They also interact, with the largest effect of sleep on emotional memory being seen when stress occurs shortly before or after encoding. Slow wave sleep (SWS) is critical for long-term episodic memory, facilitated by the temporal coupling of slow oscillations and sleep spindles. Prior work in humans has shown these associations for neutral information in non-stressed participants. Whether coupling interacts with stress to facilitate emotional memory formation is unknown. Here, we addressed this question by reanalyzing an existing dataset of 64 individuals. Participants underwent a psychosocial stressor (32) or comparable control (32) prior to the encoding of 150-line drawings of neutral, positive, and negative images. All participants slept overnight with polysomnography, before being given a surprise memory test the following day. In the stress group, time spent in SWS was positively correlated with memory for images of all valences. Results were driven by those who showed a high cortisol response to the stressor, compared to low responders. The amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral and emotional memory in the stress group only. The association with emotional memory was significantly stronger than for neutral memory within the stress group. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory.

neuroscience↗

bioRxiv2020

Sleep spindles facilitate selective memory consolidation

Sleep has been shown to be critical for memory consolidation, with some research suggesting that certain memories are prioritized for consolidation. Initial strength of a memory appears to be an important boundary condition in determining which memories are consolidated during sleep. However, the role of consolidation-mediating oscillations, such as sleep spindles and slow oscillations, in this preferential consolidation has not been explored. Here, 54 human participants (76% female) studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again six hours later. Thirty-six had a two-hour nap opportunity following learning, whilst the remaining 18 remained awake throughout. Results showed that across six hours awake, weakly encoded memories deteriorated the fastest. In the nap group however, this effect was attenuated, with forgetting rates equivalent across encoding strengths. Within the nap group, consolidation of weakly encoded items was associated with fast sleep spindle density during non-rapid eye movement sleep. Moreover, sleep spindles that were coupled to slow oscillations predicted the consolidation of weak memories independently of uncoupled sleep spindles. These relationships were unique to weakly encoded items, with spindles not correlating with memory for intermediate or strong items. This suggests that sleep spindles facilitate memory consolidation, guided in part by memory strength. Significance statementGiven the countless pieces of information we encode each day, how does the brain select which memories to commit to long-term storage? Sleep is known to aid in memory consolidation, and it appears that certain memories are prioritized to receive this benefit. Here, we found that compared to staying awake, sleep was associated with better memory for weakly encoded information. This suggests that sleep helps attenuate the forgetting of weak memory traces. Fast sleep spindles, a hallmark oscillation of non-rapid eye movement sleep, mediate consolidation processes. We extend this to show that fast spindles were uniquely associated with the consolidation of weakly encoded memories. This provides new evidence for preferential sleep-based consolidation and elucidate a physiological correlate of this benefit.

neuroscience↗