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Neither the SCN nor the adrenals are required for circadian time-place learning in mice.

Mulder CK, Papantoniou C, Gerkema MP, Van Der Zee EA - Chronobiol. Int. (2014)

Bottom Line: During Time-Place Learning (TPL), animals link biological significant events (e.g. encountering predators, food, mates) with the location and time of occurrence in the environment.Abrupt FEO phase-shifts (induced by advancing and delaying feeding time) affected TPL performance in specific test sessions while a LEO phase-shift (induced by a light pulse) more severely affected TPL performance in all three daily test sessions.We conclude that, although cTPL is sensitive to timing manipulations with light as well as food, neither the SCN nor the adrenals are required for cTPL in mice.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Neurobiology and.

ABSTRACT
During Time-Place Learning (TPL), animals link biological significant events (e.g. encountering predators, food, mates) with the location and time of occurrence in the environment. This allows animals to anticipate which locations to visit or avoid based on previous experience and knowledge of the current time of day. The TPL task applied in this study consists of three daily sessions in a three-arm maze, with a food reward at the end of each arm. During each session, mice should avoid one specific arm to avoid a foot-shock. We previously demonstrated that, rather than using external cue-based strategies, mice use an internal clock (circadian strategy) for TPL, referred to as circadian TPL (cTPL). It is unknown in which brain region(s) or peripheral organ(s) the consulted clock underlying cTPL resides. Three candidates were examined in this study: (a) the suprachiasmatic nucleus (SCN), a light entrainable oscillator (LEO) and considered the master circadian clock in the brain, (b) the food entrainable oscillator (FEO), entrained by restricted food availability, and (c) the adrenal glands, harboring an important peripheral oscillator. cTPL performance should be affected if the underlying oscillator system is abruptly phase-shifted. Therefore, we first investigated cTPL sensitivity to abrupt light and food shifts. Next we investigated cTPL in SCN-lesioned- and adrenalectomized mice. Abrupt FEO phase-shifts (induced by advancing and delaying feeding time) affected TPL performance in specific test sessions while a LEO phase-shift (induced by a light pulse) more severely affected TPL performance in all three daily test sessions. SCN-lesioned mice showed no TPL deficiencies compared to SHAM-lesioned mice. Moreover, both SHAM- and SCN-lesioned mice showed unaffected cTPL performance when re-tested after bilateral adrenalectomy. We conclude that, although cTPL is sensitive to timing manipulations with light as well as food, neither the SCN nor the adrenals are required for cTPL in mice.

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Baseline TPL performance and session skipping results. (a) Baseline TPL performances of the different groups when tested in the different light regimes. Baseline performance is defined as average performance on normal testing days, excluding the learning phase (first three days) and days on which manipulations (sessions skips) were performed. Batches were pooled for data from the same group and light regime. (b) Average TPL performances of the groups after multiple (different) session skips in the different light regimes. Performance was measured in the single next session after the skipped session. In both panels, chance level is indicated by the horizontal line. Error bars represent SEM. All results were significantly above chance level (# indicates p < 0.01, for unmarked bars p < 0.001).
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f6: Baseline TPL performance and session skipping results. (a) Baseline TPL performances of the different groups when tested in the different light regimes. Baseline performance is defined as average performance on normal testing days, excluding the learning phase (first three days) and days on which manipulations (sessions skips) were performed. Batches were pooled for data from the same group and light regime. (b) Average TPL performances of the groups after multiple (different) session skips in the different light regimes. Performance was measured in the single next session after the skipped session. In both panels, chance level is indicated by the horizontal line. Error bars represent SEM. All results were significantly above chance level (# indicates p < 0.01, for unmarked bars p < 0.001).

Mentions: The potential use of non-circadian strategies can be identified by skipping sessions and testing in absence of a LD cycle (Mulder et al., 2013a, 2013c). Baseline TPL performances in the different light regimes are shown in Figure 6(a). Baseline performance is defined as average performance on normal testing days, excluding the first three days of the learning curve and days on which manipulations (sessions skip) were performed. Batches were pooled for data from the same group/light regime). In the upcoming statistical comparisons to chance level (by two tailed one sample t-tests), the number of included subjects (N) is indicated per batch (N = Nbatch1 + Nbatch2). The same format is applied for the number of included days. In LD, performance of all groups was significantly different from chance level (SHAM: n = 4 + 4, days = 7 + 4, p < 0.0001; SCNx: n = 5 + 5, days = 7 + 4, p < 0.0001; ADX: n = 0 + 7, days = 0 + 3, p < 0.0001. Also in LL, all groups performed significantly above chance level (SHAM: n = 0 + 4, days = 0 + 3, p = 0.006; SCNx: n = 0 + 5, days = 0 + 3, p < 0.0001; ADX: n = 0 + 7, days = 0 + 3, p < 0.0001. Also in DD, both tested groups performed significantly above chance level (SHAM: n = 4 + 4, days = 3 + 5, p = 0.009; SCNx: n = 5 + 5, days = 3 + 5, p < 0.0001). We did observe that SHAM mice showed a small decline (but not significant) in average performance during testing in DD, as is reflected in a slightly lower average baseline performance for this group. No differences were found between the groups in any of the light regimes (one-way ANOVA F = 1.52, df = 9, p = 0.17; Bonferroni posttests p ≥ 0.1 for all comparisons). SHAM and SCNx mice from the ADX group were tested as separate groups, indicating no differences.Figure 6.


Neither the SCN nor the adrenals are required for circadian time-place learning in mice.

Mulder CK, Papantoniou C, Gerkema MP, Van Der Zee EA - Chronobiol. Int. (2014)

Baseline TPL performance and session skipping results. (a) Baseline TPL performances of the different groups when tested in the different light regimes. Baseline performance is defined as average performance on normal testing days, excluding the learning phase (first three days) and days on which manipulations (sessions skips) were performed. Batches were pooled for data from the same group and light regime. (b) Average TPL performances of the groups after multiple (different) session skips in the different light regimes. Performance was measured in the single next session after the skipped session. In both panels, chance level is indicated by the horizontal line. Error bars represent SEM. All results were significantly above chance level (# indicates p < 0.01, for unmarked bars p < 0.001).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4219850&req=5

f6: Baseline TPL performance and session skipping results. (a) Baseline TPL performances of the different groups when tested in the different light regimes. Baseline performance is defined as average performance on normal testing days, excluding the learning phase (first three days) and days on which manipulations (sessions skips) were performed. Batches were pooled for data from the same group and light regime. (b) Average TPL performances of the groups after multiple (different) session skips in the different light regimes. Performance was measured in the single next session after the skipped session. In both panels, chance level is indicated by the horizontal line. Error bars represent SEM. All results were significantly above chance level (# indicates p < 0.01, for unmarked bars p < 0.001).
Mentions: The potential use of non-circadian strategies can be identified by skipping sessions and testing in absence of a LD cycle (Mulder et al., 2013a, 2013c). Baseline TPL performances in the different light regimes are shown in Figure 6(a). Baseline performance is defined as average performance on normal testing days, excluding the first three days of the learning curve and days on which manipulations (sessions skip) were performed. Batches were pooled for data from the same group/light regime). In the upcoming statistical comparisons to chance level (by two tailed one sample t-tests), the number of included subjects (N) is indicated per batch (N = Nbatch1 + Nbatch2). The same format is applied for the number of included days. In LD, performance of all groups was significantly different from chance level (SHAM: n = 4 + 4, days = 7 + 4, p < 0.0001; SCNx: n = 5 + 5, days = 7 + 4, p < 0.0001; ADX: n = 0 + 7, days = 0 + 3, p < 0.0001. Also in LL, all groups performed significantly above chance level (SHAM: n = 0 + 4, days = 0 + 3, p = 0.006; SCNx: n = 0 + 5, days = 0 + 3, p < 0.0001; ADX: n = 0 + 7, days = 0 + 3, p < 0.0001. Also in DD, both tested groups performed significantly above chance level (SHAM: n = 4 + 4, days = 3 + 5, p = 0.009; SCNx: n = 5 + 5, days = 3 + 5, p < 0.0001). We did observe that SHAM mice showed a small decline (but not significant) in average performance during testing in DD, as is reflected in a slightly lower average baseline performance for this group. No differences were found between the groups in any of the light regimes (one-way ANOVA F = 1.52, df = 9, p = 0.17; Bonferroni posttests p ≥ 0.1 for all comparisons). SHAM and SCNx mice from the ADX group were tested as separate groups, indicating no differences.Figure 6.

Bottom Line: During Time-Place Learning (TPL), animals link biological significant events (e.g. encountering predators, food, mates) with the location and time of occurrence in the environment.Abrupt FEO phase-shifts (induced by advancing and delaying feeding time) affected TPL performance in specific test sessions while a LEO phase-shift (induced by a light pulse) more severely affected TPL performance in all three daily test sessions.We conclude that, although cTPL is sensitive to timing manipulations with light as well as food, neither the SCN nor the adrenals are required for cTPL in mice.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Neurobiology and.

ABSTRACT
During Time-Place Learning (TPL), animals link biological significant events (e.g. encountering predators, food, mates) with the location and time of occurrence in the environment. This allows animals to anticipate which locations to visit or avoid based on previous experience and knowledge of the current time of day. The TPL task applied in this study consists of three daily sessions in a three-arm maze, with a food reward at the end of each arm. During each session, mice should avoid one specific arm to avoid a foot-shock. We previously demonstrated that, rather than using external cue-based strategies, mice use an internal clock (circadian strategy) for TPL, referred to as circadian TPL (cTPL). It is unknown in which brain region(s) or peripheral organ(s) the consulted clock underlying cTPL resides. Three candidates were examined in this study: (a) the suprachiasmatic nucleus (SCN), a light entrainable oscillator (LEO) and considered the master circadian clock in the brain, (b) the food entrainable oscillator (FEO), entrained by restricted food availability, and (c) the adrenal glands, harboring an important peripheral oscillator. cTPL performance should be affected if the underlying oscillator system is abruptly phase-shifted. Therefore, we first investigated cTPL sensitivity to abrupt light and food shifts. Next we investigated cTPL in SCN-lesioned- and adrenalectomized mice. Abrupt FEO phase-shifts (induced by advancing and delaying feeding time) affected TPL performance in specific test sessions while a LEO phase-shift (induced by a light pulse) more severely affected TPL performance in all three daily test sessions. SCN-lesioned mice showed no TPL deficiencies compared to SHAM-lesioned mice. Moreover, both SHAM- and SCN-lesioned mice showed unaffected cTPL performance when re-tested after bilateral adrenalectomy. We conclude that, although cTPL is sensitive to timing manipulations with light as well as food, neither the SCN nor the adrenals are required for cTPL in mice.

Show MeSH