Hippocampal sharp-wave ripples correlate with periods of naturally occurring self-generated thoughts in humans

Human cognition frequently involves focusing on information unrelated to the immediate environment, a phenomenon known as mind wandering. This can account for up to 30% of our waking thoughts and is linked to various aspects of mental health and cognitive function. Neuroimaging studies suggest involvement of the default mode network, particularly the posterior cingulate and medial prefrontal cortex. Individual differences in medial temporal lobe anatomy also correlate with mind-wandering tendencies. While these studies highlight the brain regions involved, the precise mechanisms driving self-generated thoughts remain unclear. This study proposes that hippocampal sharp-wave ripples (SWRs), bursts of synchronized neuronal activity, play a key role in generating these self-generated cognitive states. SWRs are associated with memory consolidation during sleep and are also observed during wakefulness, with activity levels varying with the animal's behavioral state. The researchers aim to investigate the relationship between SWRs and naturally occurring ongoing thoughts in humans to test this hypothesis.

Existing research demonstrates a strong correlation between self-generated thought processes and activity in brain regions like the posterior cingulate cortex and medial prefrontal cortex, key components of the default mode network. Studies also point to a relationship between individual differences in medial temporal lobe structure and the frequency and characteristics of self-generated thoughts, both in laboratory settings and in daily life. However, little is known about the precise neural mechanisms orchestrating these experiences. The current study builds on the hypothesis that these experiences may be linked to hippocampal functions, particularly the role of the hippocampus in memory, prospection, and the broader organization of cortical function, suggesting SWRs may be a critical component of this process.

Ten epilepsy patients with intracranial electrodes implanted in or near their hippocampus for presurgical evaluation participated in the study. Long-term EEG recordings (9-15 days) were collected while patients engaged in their normal daily activities in a monitored room. Participants completed hourly questionnaires assessing their thoughts and feelings using a modified Daydreaming Experience Scale (mDES), covering dimensions like task focus, future/past orientation, self-referential content, emotional valence, vividness, and imagery. Simultaneously, physiological data (electrodermal activity, acceleration, blood volume pulse, interbeat interval) were recorded using a wearable device. Hippocampal local field potentials (LFPs) were analyzed to detect SWRs using a previously established method. Data were preprocessed to remove artifacts and noise. The relationship between SWR rates and both the mDES responses and physiological measures was analyzed using general linear mixed-effects models, incorporating individual differences as random effects. Statistical significance was assessed using one-way ANOVA, Pearson/Spearman correlation, and permutation tests.

The study found significant diurnal fluctuations in hippocampal SWR rates, with lower rates around mealtimes and increased activity in the afternoon compared to the morning. SWR rates were positively correlated with delta wave amplitude, an indicator of slow-wave sleep. Importantly, higher SWR rates were associated with longer periods where participants reported thoughts that were vivid, less desirable, more imaginable, and less related to external tasks. The analysis also showed a weak but significant correlation between SWR rates and certain physiological parameters (electrodermal activity and acceleration), particularly around the time of SWR events, suggesting a potential link with arousal levels. However, these physiological measures did not explain the variability in SWR activity fully. The study revealed that the mDES responses were more strongly correlated with SWRs in the period preceding the questionnaire responses than during the actual response time, indicating that the SWRs are likely more closely tied to the generation of thoughts rather than the act of reporting them.

The findings strongly support the hypothesis linking hippocampal SWRs to naturally occurring self-generated thoughts. The association between higher SWR rates and less task-focused, more vivid, and less desirable thoughts aligns with previous research on the role of the medial temporal lobe in self-generated cognition. The diurnal pattern of SWRs observed is consistent with the known association of SWRs with sleep cycles, but other factors, such as mealtimes and blood glucose levels, also seem to play a role. The lack of a strong association between SWRs and physiological measures suggests that the link between SWRs and self-generated thoughts is not solely driven by changes in arousal levels. This study emphasizes the importance of experience sampling methods, like mDES, in bridging the gap between brain activity and the subjective experience of thought. The results contribute to a broader understanding of how the hippocampus, through SWRs, actively participates in shaping the rich tapestry of our internal mental life.

This study provides compelling evidence linking hippocampal sharp-wave ripples (SWRs) to the content and characteristics of self-generated thoughts in humans. The association between SWRs and vivid, less desirable, and task-unrelated thoughts supports the growing understanding of the medial temporal lobe's role in internally driven cognition. Future research should explore the causal relationship between SWRs and self-generated thoughts, potentially using pharmacological interventions or targeted stimulation techniques. Furthermore, extending the study to larger and more diverse populations, including healthy individuals, is crucial for generalizing these findings and understanding the implications for various cognitive and clinical conditions, including those involving intrusive thoughts.

The study's reliance on intracranial EEG recordings from epilepsy patients is a significant limitation. The presence of epilepsy and medication could potentially influence SWR activity and thought patterns. While efforts were made to exclude data during epileptic seizures and account for medication effects, the possibility of residual influences cannot be fully ruled out. The hospital setting might have restricted the range of activities and therefore the diversity of thought patterns experienced by participants. The correlational nature of the findings limits causal inferences; future research involving manipulations of SWRs or other interventions is necessary to establish causality. Finally, the use of a relatively small sample size limits the generalizability of the results.