1. Neuroscience

Regional response to light illuminance across the human hypothalamus

  1. Islay Campbell
  2. Roya Sharifpour
  3. Jose Fermin Balda Aizpurua
  4. Elise Beckers
  5. Ilenia Paparella
  6. Alexandre Berger
  7. Ekaterina Koshmanova
  8. Nasrin Mortazavi
  9. John Read
  10. Mikhail Zubkov
  11. Puneet Talwar
  12. Fabienne Collette
  13. Siya Sherif
  14. Christophe Phillips
  15. Laurent Lamalle
  16. Gilles Vandewalle  Is a corresponding author
  1. GIGA-CRC Human Imaging, University of Liège, Belgium
  2. Faculty of Health, Medicine and Life Sciences, School for Mental Health and Neuroscience, Alzheimer Centre Limburg, Maastricht University, Netherlands
  3. Synergia Medical SA, Belgium
  4. Institute of Neuroscience (IoNS), Department of Clinical Neuroscience, Université Catholique de Louvain (UCLouvain), Belgium
https://doi.org/10.7554/eLife.96576.3
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  1. Islay Campbell
  2. Roya Sharifpour
  3. Jose Fermin Balda Aizpurua
  4. Elise Beckers
  5. Ilenia Paparella
  6. Alexandre Berger
  7. Ekaterina Koshmanova
  8. Nasrin Mortazavi
  9. John Read
  10. Mikhail Zubkov
  11. Puneet Talwar
  12. Fabienne Collette
  13. Siya Sherif
  14. Christophe Phillips
  15. Laurent Lamalle
  16. Gilles Vandewalle
(2024)
Regional response to light illuminance across the human hypothalamus
eLife 13:RP96576.
https://doi.org/10.7554/eLife.96576.3
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4 figures, 4 tables and 2 additional files

Figures

Figure 1
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Experimental protocol.

(A) Overall timeline. After prior light history standardisation, participants performed executive (always first), emotional and attentional tasks (pseudo-randomly 2nd or 3rd, blue arrow). As the attentional task included fewer light conditions, it is not considered in the present manuscript (see Materials and methods for more details). (B) Spectral power distribution of light exposures. Monochromatic orange: 0.16 mel EDI lux; Polychromatic, blue-enriched light (6500 K); LOW, MID, HIGH: 37, 92, 190 mel EDI lux. For the present analyses, we discarded colour differences between the light conditions and only considered illuminance as indexed by mel EDI lux, constituting a limitation of our study. See Supplementary file 1b for full details). (C, D) Tasks procedures. Time is reported in seconds relative to session onset; participants were pseudo-randomly exposed to the 4 light conditions. (C) Executive task: alternation of letter detection blocks (0-back) and working memory blocks (2-back). (D) Emotional task: lure gender discrimination of vocalisations (50% angry (red), 50% neutral (white).

Figure 2
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Illuminance impact on the hypothalamus subparts.

(A) Segmentation of the hypothalamus in five subparts in a representative participant. The nuclei encompassed by the different subparts are indicated in the right inset – according to Billot et al., 2020. ARC: arcuate nucleus; DMH; dorsomedial nucleus; LH lateral hypothalamus; LTN: lateral tubular nucleus; MB: mamillary body; POA: preoptic area; PVN: paraventricular nucleus; PNH: posterior nucleus of the hypothalamus; SCN: suprachiasmatic nucleus; SON: supraoptic nucleus; TMN: tuberomammillary nucleus; VMN: ventromedial nucleus. (B, C) Estimates (beta; arbitrary unit – a.u.) of the collective impact of illuminance variation on the activity of each hypothalamus subpart (Refer to Table 1 full statistics). (B) Executive task: significant main effect of hypothalamus subparts (p=0.002), no significant main of task type (p=0.4) or subpart-by-task-type interaction (p=0.61). (C) Emotional task: significant main effect of hypothalamus subparts (p<0.0001), and of stimulus type (p=0.048) or subpart-by-stimulus-type interaction (p=0.74). (D–G) Whole brain analyses of the collective impact of the variations in illuminance over the hypothalamus area - for illustration. A local positive peak (red; puncorrected <0.001) was detected over the posterior hypothalamus subpart (light blue) in executive (E) and emotional (G). A local negative peak (red; puncorrected <0.001) was detected over the inferior-tubular hypothalamus subparts (light orange) during the executive task (D), while local negative peak (red; puncorrected <0.001) was detected over the inferior-anterior (yellow) and superior-anterior (blue) hypothalamus subparts during the emotional task (F) – insets correspond to enlargements over the hypothalamus area. Arrows from panels B and C arise from and are colour coded according to the hypothalamus subpart that is displayed in panels D to G. These results indicate that our finding does not arise from a nearby ‘leaking’ activation/deactivation. (H–K) Estimates of the impact of each illuminance on the activity of the hypothalamus subparts. (Refer for Table 2 and Supplementary file 1c–f for full statistics) Activity dynamics across illuminance for each subpart (colour code as in A). Results are displayed per task or stimulus type although no interactions with task or stimulus type were detected. Significant illuminance-by-hypothalamus-subpart interactions were detected for (H, I) the executive task (p=0.041) and (J, K) the emotional task (p=0.041). Small letter indicate significant difference (p<0.05) between the following subparts at illuminance: a. 92 mel EDI lux: posterior vs. superior-anterior & inferior-tubular; b. 190 mel EDI lux: posterior vs. inferior-anterior, superior-anterior and inferior-tubular; c. 0 mel EDI lux: posterior vs. superior-tubular; d. 92 mel EDI lux: posterior vs. superior-anterior; superior-anterior vs. superior-tubular; e. 190 mel EDI lux: posterior vs. inferior-anterior, superior-anterior and inferior-tubular; superior-tubular vs. superior-anterior, inferior-tubular and inferior-anterior. Means +- standard deviations are plotted.

Figure 3
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Impact of illuminance on performance and relationships with the activity of the posterior hypothalamus subpart.

(A) Accuracy (percentage of correct responses) to the 2-back increased with increasing illuminance (p=0.034). (B) Accuracy to the 2-back task is negatively correlated to the activity of the posterior hypothalamus subpart (p=0.0027). (C, D) Accuracy to the 2-back task is not correlated to the activity of the inferior-anterior (C) and inferior-tubular (D) hypothalamus subparts (p>0.4). Association between superior-anterior and superior-tubular subparts are not displayed but were not significant (p>0.6). See Supplementary file 1g for full details. (E) Accuracy to the 0-back task is not correlated to the activity of the posterior hypothalamus subpart (p=0.45). (F) Reaction times to the emotional stimuli did not significantly change with increasing illuminance (p=0.41). (G) Reaction times to the emotional stimuli are correlated to the activity of the posterior hypothalamus subpart (p=0.04) with higher activity associated to slower reaction times. (H) Reaction times to the neutral stimuli are not correlated to the activity of the posterior hypothalamus subpart (p=0.6). Box plots: horizontal line = median; box = higher/lower quartiles: vertical line = maximum/minimum. Regression plots: solid and dashed lines correspond to the significant and not significant linear regression lines, respectively.

Author response image 1
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Activity estimate variability per hypothalamus subpart and subpart size.

Tables

Table 1
Differences between hypothalamus subparts in the collective impact of the variation in illuminance on their activity.
Executive task
Main GLMMPairwise comparisons
EffectF value (df)p value*Partial R2Contrast†t-valuePuncorrectedPcorrected
Hypothalamus subparts4.36 (4,225)0.0020.081 vs 2–0.300.760.99
1 vs 3–3.480.00060.0056
1 vs 4<0.010.991
Task0.74 (1,25)0.41 vs 5–0.570.570.98
Hypothalamus subparts x task type0.68 (4,225)0.612 vs 3–3.170.00170.015
2 vs 40.310.760.99
2 vs 5–0.270.790.99
Age0.33 (1,22)0.573 vs 43.480.00060.0055
BMI0.59 (1,22)0.453 vs 52.540.00410.033
Sex0.01 (1,22)0.914 vs 5–0.50.570.98
Emotional task
Main GLMMPairwise comparisons
EffectF Valuep value*Partial R2Contrast†t-valuePuncorrectedPcorrected
Hypothalamus subparts9.38 (4,194)<.00010.221 vs 20.670.670.99
1 vs 3–4.76<0.0001<0.0001
1 vs 40.000.991
Task4.33 (1,25)0.0480.151 vs 5–1.880.060.33
Hypothalamus subparts x stimulus type0.5 (4,194)0.742 vs 3–5.43<0.00010.0001
2 vs 4–0.660.510.96
2 vs 5–2.540.0120.086
Age0.43 (1,22)0.523 vs 44.76<0.0001<0.0001
BMI0.05 (1,22)0.833 vs 52.850.00480.038
Sex1.47 (1,22)0.244 vs 5–1.880.0610.32

  1. Outputs of the generalized linear mixed model (GLMM) with subject as the random factor (intercept and slope), and task and subpart as repeated measures (ar(1) autocorrelation).

  2. *

    The corrected p-value for multiple comparisons over 2 tests is p < 0.025.

  3. †

    Refer to Figure 2A for correspondence of subpart number.

Table 2
Statistical outputs of GLMM testing for differences between the activity of each subpart of the hypothalamus under each illuminance.
Executive task
Main GLMMComparisons between subparts per illuminance†
EffectF-value (df)P valuePartial R²Illuminance*contrastt-valuep-value
Subpart1.4 (4,228)0.23922 vs 3–2.250.025
Illuminance2.15 (4,1017)0.073923 vs 42.580.01
1901 vs 3–2.800.0053
Task3.24 (1,228)0.0731902 vs 3–2.240.025
Subpart x Illuminance1.7 (16,1017)0.0410.091903 vs 43.150.0017
Age1.19 (1,22)0.29
BMI0.01 (1,22)0.9
Sex0.38 (1,22)0.54
Emotional task
Main GLMMComparisons between subparts per illuminance†
EffectF-value (df)p valuePartial R²Illuminance*contrastt-valuep-value
Subpart4.29 (4,229)0.00230.0703 vs 5–2.050.04
922 vs 3–2.530.012
Illuminance9.41 (4,1020)<0.00010.035922 vs 5–2.960.0032
1901 vs 3–3.310.001
1902 vs 3–4.75<0.0001
Task0.13 (1,229)0.721901 vs 5–2.50.013
1902 vs 5–4.04<0.0001
1903 vs 43.130.0018
Subpart x Illuminance1.7 (16,1020)0.0410.0261904 vs 5–2.320.021
Age0.59 (1,22)0.45
BMI1.54 (1,22)0.23
Sex0.05 (1,22)0.83
  1. *

    illuminance in mel EDI lux.

  2. †

    Only significant comparisons are reported in the main text. For the full table, including post hocs comparing light levels within a subpart, refer to Supplementary file 1c–g.

Author response table 1
Recomputations of the main GLMMs using subpart sizes rather than subpart numbers as covariate of interest.
Executive task
Main GLMM
EffectF value
(df)		P value*Partial R ^(2)
Subpart size4.36,(4,200)0.00210.08
Task0.74,(1,25)0.4
Subpart size x
task type		0.68,(4,200)0.61
Age0.33,(1,22)0.57
BMI0.59,(1,22)0.45
Sex0.01,(1,22)0.91
Emotional task
Main GLMM
EffectF ValueP value*Partial R ^(2)
Subpart size9.64,(4,193)< .00010.17
Task4.55,(1,25)0.0430.15
Subpart size x
stimulus type		0.41,(4,193)0.8
Age0.4(1,22)0.53
BMI0.02,(1,22)0.89
Sex1.37,(1,22)0.25
Author response table 2
Difference in activity estimate standard deviation between hypothalamus subparts during the n-back task.
Subpart number (GLMM)
EffectF value
(df)		P value ^(**)Partial R ^(2)
Hypothalamus
subparts		32.3
(4,260)		< 0.00010.33
Task< 0.001
(1,23)		0.97
Hypothalamus
subparts x task
type		0.03
(4,260)		0.99
Post hocs
subpartT valuepP
1 vs. 25.24< .0001< .0001
1 vs. 30.300.770.99
1 vs. 41.470.140.58
1 vs. 5-5.92< .0001< .0001
2 vs. 3-4.95< .0001< .0001
2 vs. 4-3.770.00020.0019
2 vs. 5-11.17< .0001< .0001
3 vs. 41.180.240.77
3 vs. 5-6.22< .0001< .0001
4 vs. 5-7.39< .0001< .0001

Additional files

Supplementary file 1

Online supplementary information.

(a) Demographics of study sample. (b) Light characteristics. (c) Post hoc contrasts between illuminances within each hypothalamus subpart during the executive task. (d) Post hoc contrasts between illuminances within each hypothalamus subpart during the emotional task. (e) Post hoc contrasts between hypothalamus subpart for each illuminance during the executive task. (f) Post hoc contrasts between hypothalamus subpart for each illuminance during the emotional task. (g) Association between performance to the 2-back task and the activity of each hypothalamus subpart during each illuminance.

https://cdn.elifesciences.org/articles/96576/elife-96576-supp1-v1.docx
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  1. Islay Campbell
  2. Roya Sharifpour
  3. Jose Fermin Balda Aizpurua
  4. Elise Beckers
  5. Ilenia Paparella
  6. Alexandre Berger
  7. Ekaterina Koshmanova
  8. Nasrin Mortazavi
  9. John Read
  10. Mikhail Zubkov
  11. Puneet Talwar
  12. Fabienne Collette
  13. Siya Sherif
  14. Christophe Phillips
  15. Laurent Lamalle
  16. Gilles Vandewalle
(2024)
Regional response to light illuminance across the human hypothalamus
eLife 13:RP96576.
https://doi.org/10.7554/eLife.96576.3