Seasonality in human cognitive brain responses

Obvious seasonal changes are observed in animals: hibernation, migration or reproduction for instance. In humans even if it is maybe less obvious, several variables are also affected by season changes: conception, blood pressure, neurotransmitters or mood for example. Even if we know that light has a positive impact on seasonal affective disorder (SAD) and is able to enhance cognition, the effect of seasonal variation in photoperiod (day length) on cognition has been poorly investigated, leading to inconsistent results. However, in our societies asking for constant optimal functioning throughout the year, investigating the impact of seasons on brain functions is essential. Understanding the mechanisms underlying seasonal variation in brain responses could lead to the development of strategy to counteract potential intra-individual differences across the year, as observed in seasonal affective disorder. The fact that brain bases of seasonality in human cognition remain elusive may arise in part from the fact that genuine seasonal rhythms of human brain function are difficult to measure due to a number of factors which could directly affect brain function: light exposure, sleep/wake rhythm, external temperature, food intake, physical exercise, social interactions.Therefore, to investigate these questions we performed two experiments under really strictly controlled conditions, free of seasonal cues in young healthy volunteers. By using functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation coupled to electroencephalography (TMS – EEG) we assessed the effect of seasonal change on brain function and cognition. Our data show that brain responses vary significantly across seasons but surprisingly the pattern of the rhythm was task-dependent, revealing a previously unappreciated process-specific seasonality in human cognitive brain function. Indeed, brain responses to a sustained attention task had maximum and minimum responses around summer and winter solstices, respectively, while for a working memory task, maximum and minimum responses were observed around autumn and spring equinoxes. In a second experiment, we observed an earlier peak of macroscopic EEG variables (TMS cortical excitability, gamma EEG activity) in their daily 24h profile under short photoperiod (fall and winter) compared to long photoperiod (spring and summer). Computational analyses revealed that these changes were likely triggered by an earlier peak of the GABA/glutamate balance. The latter results speak for a role of the balance between inhibition and excitation in seasonal encoding in human, as suggested in rodent suprachiasmatic nuclei hosting the master circadian clock. Moreover, these results were observed after at least nearly 2 days under a protocol free of seasonal cues, meaning that our specie may have its own kind of physiological memory for previous photoperiod. Importantly, task performances were not significantly impacted by these seasonal variations in brain function and were thus constant throughout the year. In addition, the functional link between the mesoscopic level (GABA/Glutamate balance) and the macroscopic brain markers (TMS cortical excitability, gamma EEG activity) is stable throughout the year. Therefore, our data suggest that seasonal changes in environmental factors impact the human brain through plasticity at the neuronal network level. Adaptation at the fast milliseconds range may confer stability at the macroscopic brain level to maintain behavior constant. Based on these results we hypothesized that persons with less neuronal plasticity/adaptation may undergo dysfunction at the macroscopic level. This could explain in part the heterogeneity of the responses to seasonal changes through the population (for instance why some people suffer from seasonal affective disorder and other do not).