Seasonality in human cognitive brain responses

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Fig 1 Schematic representation of the protocol Following an 8 h baseline night of sleep in complete darkness participants underwent a 42 h sleep deprivation under. constant routine conditions in dim light 5 lx 19 C semirecumbent position regular liquid isocaloric food intake no time cues sound proofed room They were then. given a 12 h recovery sleep opportunity in darkness an hour after which they completed fMRI recordings red star Functional MRI recordings were completed while. lying down in darkness and included PVT and n back tasks Relative clock time for participants habitually waking up at 8 00 AM Striped blue box during sleep dep. rivation represents the habitual sleep period The figure represents the last 2 5 d of the protocol see Fig S1 for a description of the entire in laboratory experiment. Results and Discussion conducted in Li ge Belgium latitude 50 633 N longitude 5 567 E. Twenty eight young healthy participants age 21 1 5 y mean between May 2010 and October 2011 They were instructed to. SD 14 women Table S1 took part in a cross sectional study follow a regular sleep wake schedule for 3 wk before a 4 5 d. NEUROSCIENCE, Fig 2 Seasonal variations in brain activity associated with sustained attention A Significant pcorrected 0 05 seasonal variations in PVT brain responses displayed over the. mean structural image of all participants display at puncorrected 0 001 Only clusters 30 voxels are displayed see Table 1 for full results Vertical color bar corresponds to F test. values B Double plot of PVT brain response estimates in regions of A in a sinusoidal representation Day 1 corresponds to January 1 First letter of each month is displayed on. top Thickblackline corresponds to averageof all responseestimates Gray arearepresents daily daylength in minutes in Li ge C Same as B in polar coordinates arrow length. Downloaded by guest on September 12 2020, represents seasonal variation amplitude One degree is roughly equal to 1 d 360 for 365 d Maximum responses were located between 152 and 188 mean 168 9 i e June 3. and July 9 mean June 20 D Double plot of individual activity estimates in a representative region of A amygdala and its sinusoidal fit red line E Seasonal environmental. factors recorded in Li gein 2011 temperature Celsius degrees blue humidity percent red daylength minutes green andday to day day length gain loss minutes violet. Meyer et al PNAS March 15 2016 vol 113 no 11 3067, Table 1 Seasonal variation in PVT brain responses cognition change with time of year We hypothesize that the. Brain areas Side XYZ Z score P value seasonality in brain responses could predict some of the seasonal. variations in performance previously reported for potentially. Frontoorbital gyrus L 38 54 6 3 43 0 017 more sensitive tasks 11 13. L 26 52 10 3 56 0 012 We next investigated whether other behavioral and physiologi. Medial frontoorbital gyrus R 10 56 12 3 34 0 022 cal variables could account for the observed annual variations in. Superior frontopolar gyrus L 26 60 20 4 32 0 01 PVT brain responses Subjective and objective neurophysiological. Superior frontal gyrus L 14 20 64 4 56 0 01 measures of alertness and subjective assessments of affective di. Middle frontal gyrus L 50 18 38 3 29 0 025 mensions acquired immediately before fMRI acquisitions did not. Pre SMA R 2 20 48 3 11 0 042 change significantly across seasons In addition in our dataset we. Posterior cingulate gyrus L 4 42 22 3 10 0 042 could not replicate seasonal changes in melatonin secretion profile. Precuneus L 18 50 36 3 50 0 014 that were reported in some 30 33 but not all 34 35 publi. Supramarginal gyrus L 56 36 30 3 93 0 004 cations P 0 05 Table S2 Only self reported mood varied. Intraparietal sulcus L 30 46 34 3 29 0 025 significantly over season P 0 003 Table S2 but this variation. R 30 42 36 3 37 0 021 was not significantly related to the seasonal changes in brain re. Superior temporal sulcus L 48 58 16 3 45 0 016 sponses Table 1 and Fig S3 In summary sustained attention. Temporal pole L 38 16 36 4 66 0 05 related brain activity fluctuates across seasons but these changes. Fusiform gyrus R 50 56 20 3 74 0 007 were not related to variations in the behavioral endocrine or. R 42 58 18 3 12 0 039 neurophysiological parameters assessed in our study. Parahippocampal gyrus L 32 28 24 4 61 0 05 Photoperiod is the most obvious factor associated with season. Hippocampus R 28 14 24 4 58 0 05 and both the intensity and spectral composition of light to which. Caudate nucleus L 6 4 4 3 23 0 030 people are exposed vary with season 36 Fig 2 indeed suggests. Amygdala L 22 10 24 4 87 0 05 that PVT brain responses were closely related to photoperiod. Globus pallidus R 18 2 0 4 21 0 001 gray area Fig 2B A formal analysis revealed that all PVT brain. Thalamus R 10 6 8 3 86 0 005 responses showing seasonal variations were significantly associated. L 8 8 10 3 79 0 006 with day length This finding could imply that there is a physio. logical memory for the photoperiod to which participants were. P values corrected for multiple comparisons over a priori small volume of. interests except corrected over the entire brain X Y Z coordinates millime. exposed before admission to the laboratory Indeed before fMRI. ters in Montreal Neurological Institute stereotactic space All regions survived recordings participants had not seen sunlight for 4 5 d and had. to an inclusive mask puncorrected 0 001 consisting of a brain map of the been for 63 h in dim light during wakefulness and in darkness. potential PVT brain responses covarying with day length suggesting that an during sleep episodes Consistently effects of prior light exposure. nual variations in all regions are significantly driven by the seasonal changes in photic memory on cognitive brain responses have formerly. day length No region survived to an inclusive mask puncorrected 0 001 been demonstrated on a much shorter timescale in humans 37. whereas all regions survived exclusive masking puncorrected 0 05 with a brain and photoperiod memory has previously been described as after. map of the potential executive brain responses covarying i subjective mood effects of photoperiod on circadian clock neurons in rodents 38. and ii PVT performance median 20 fastest 20 slowest reaction times. Whether our data reflect a true human photoperiod memory is. suggesting that annual variations in all regions are not significantly driven by. the seasonal changes in these variables L left R right. however not possible to ascertain because many other environ. mental factors covary with season and photoperiod including air. temperature and humidity Fig 2E, in laboratory protocol devoid of seasonal cues Figs S1 and S2 Having established seasonal annual variations in sustained. Functional MRI fMRI recordings were acquired 1 h after wake attention related brain responses we then examined whether. up time following 63 h of strictly controlled experimental condi such variations could be generalized to other cognitive domains. tions Fig 1 Each recording included a sustained attention task by considering the n back task implemented in our protocol We. visual psychomotor vigilance task PVT 21 and a higher order found that brain responses to this executive task varied signifi. executive function task auditory n back task involving storage cantly with season in the thalamus including the pulvinar and in. updating and comparison of information in working memory 22 prefrontal and frontopolar areas similar to the PVT results In. We first focused on the brain responses induced by the PVT addition significant annual variation was observed in the insula. and found significant annual variations in areas involved in alert a brain region involved in executive processes attention and. ness thalamus 23 and amygdala 24 and in executive control affective regulation 39 Fig 3A and Table 2 Compared with. PVT brain responses significant seasonal variations seemed to. frontal areas 25 and hippocampus 26 Fig 2A and Table 1. encompass a reduced set of brain areas which could indicate a. Seasonal variations were also detected in the globus pallidus. relative decrease in seasonality on executive brain responses in. parahippocampal gyrus fusiform gyrus supramarginal gyrus and line with previous suggestions of a reduced seasonal impact on. in the temporal pole recruited during PVT execution 27 28 and behavioral measures of more complex tasks 13. in the precuneus involved in visuospatial attention 29 As pos This qualitative task specific difference was complemented by a. tulated extraction of the seasonal variations in PVT brain re statistically significant difference in the dynamics of brain response. sponses revealed a similar rhythm in all these brain regions with estimates across the year with maximum and minimum responses. maximal responses around mid June and minimal around mid being located 3 mo later for the n back compared with the. December i e around solstices Fig 2B PVT i e around autumn and spring equinoxes respectively. Variations in PVT brain responses were not related to sig Fig 3 B and C day of the year at responses maximum phase. nificant changes in PVT performance which remained good and PVT 168 9 8 2 n back 265 7 13 t11 20 16 P 0 001. stable throughout the year P 0 2 Table S2 This guarantees Similar to the PVT performance on the n back was good and. that fMRI differences were not significantly biased by differences stable throughout the year in our sample Table S2 However. in performance to the task and suggests that fMRI is more covariation with photoperiod was not significant for any of the. sensitive than the behavioral tests we used in identifying seasonal executive brain responses that significantly varied with season. Downloaded by guest on September 12 2020, variations in cognition Stable performance throughout the year As depicted in Fig 3 there seems however to be a striking sim.
via distinct brain dynamics implies however that the cost of ilarity between annual dynamics in executive brain responses and. cognition i e the neural resources involved in or at disposal for day to day variation in daylength i e the number of minutes of. 3068 www pnas org cgi doi 10 1073 pnas 1518129113 Meyer et al. Fig 3 Seasonal variations in executive brain activity Display as in Fig 2 A Significant pcorrected 0 05 seasonal variations in auditory three back brain. responses minus control task brain responses simple letter detection B Executive brain response estimates in regions of A Gray area represents day to day. change in photoperiod in Li ge minutes C Same as B in polar coordinates Maximum responses were located between 243 and 282 mean 265 75 i e. September 3 and October 12 mean September 22 D Double plot of individual activity estimates in a representative regions of A middle frontal region. and its sinusoidal fit red line,NEUROSCIENCE, day length gained or lost from one day to the next which peaks at and subcortical thalamus areas 44 46 similar to those de. the equinoxes This similarity is indeed confirmed statistically tected here in response to a PVT task In contrast the emerging. Table 2 As for photoperiod however factors such as air tem seasonal pattern for dopamine brain concentration is charac. perature and humidity Fig 2E covary with day to day day length terized by higher levels in fall and lower levels in spring 47 48. variations such that these are equally likely to contribute to sea that is with a pattern reminiscent of the annual variations in. sonality in cognitive brain function executive brain response observed in our sample Similarly. Overall the results provide clear evidence for seasonality in. seasonal variation in serum brain derived neurotrophic factor. diverse types of cognitive processes and suggest that the annual. dynamics are process specific One might postulate that more basic concentration a protein involved in learning and the regulation. cognitive processes such as attention are more tightly related to and plasticity of neuronal network has been reported to undergo. basic environmental changes e g day length whereas higher annual dynamics leading to higher circulating levels in the fall. cognitive processes are related to more complex cues such as for 49 Whether brain responses to learning tasks would have a. instance social interactions e g summer holidays usually en similar annual pattern as the brain activity related to a working. compass usually July and August in Belgium This speculation memory task remains to be investigated As a whole it seems. cannot be tested here but would imply that brain response sea that key modulators of brain function show at least some sea. sonal dynamics would be different in countries with different en sonality potentially contributing to the seasonal changes in. vironmental and social constraints cognitive brain response we detected. Interestingly seasonal variations have been found in mono Influence of season is broad in the animal kingdom and en. amines that are often related to cognitive functions notably at compasses locomotion body mass endocrine function melato. tention and executive processes 40 41 Seasonal changes in nin secretion pelage and sexual activity 1 50 51 Expression. serotonin levels in cerebrospinal fluid and blood as well as sero. of at least part of the human genome seems to be seasonal 7. tonin transporter binding have been repeatedly observed but not. systematically see refs 42 and 43 mostly leading to higher se speaking for a potential broad impact of season also in humans. rotonin levels in summer 19 44 45 i e with a pattern poten Our findings indicate that in addition to time of day 2 time of. seasons correspond to annual environmental fluctuations to which organisms have adapted However little is known about seasonal variations in human brain physiology We investigated annual rhythms of brain activity in a cross sectional study of healthy young participants They were maintained in an environment free of seasonal cues for 4 5 d after which brain responses were assessed using

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