Table 1.
The circadian regulation of rodent behaviors.
| Task | Animal | Treatment | Experimental Time | Intertrial interval | Results | References |
|---|---|---|---|---|---|---|
| Passive avoidance | Swiss Webster mouse | ZT time | 12:12h LD, ZT9 or 17 | 24h | Light phase groups performed better than dark ones. | (Stephens et al., 1967) |
| Passive avoidance | Rat | ZT time; melanocyte - stimulating hormone | 12:12h LD, ZT6 or 13 | 48h | Light phase groups performed better than dark ones. Melanocytes improved their performance in the dark. | (Sandman et al., 1971) |
| Passive avoidance | Sprague-Dawley rat | ZT time | 12:12h LD, every 4 h | 48h | Light phase groups performed better than dark ones. | (Davies et al., 1973) |
| Passive avoidance | Rat | ZT time; ITI | 12:12h LD, ZT2, 8, 14, 20 | 15min, 6h, 12h, 18h, 24h, 30h, 36h, 48h, 72h | 15min and all 24h groups performed better than others. | (Holloway and Wansley, 1973b) |
| Passive avoidance | Rat | ZT time; ITI | 12:12h LD, ZT1-4.5 or 5.5-8 | 30sec-36h | 30 sec, 15min, 12h, 24h, and 36h groups performed better than others. | (Wansley and Holloway, 1976) |
| Passive avoidance | Sprague-Dawley rat | ZT time; ITI | 12:12h LD; ZT1-4 or 7-10 | 15min or every 3-h up to 24h | 15min, 9h, 12h, and 24h groups performed better than others. | (Hunsicker and Mellgren, 1977) |
| Passive avoidance | Sprague-Dawley rat | SCN lesions; ITI | 12:12h LD; ZT6-7 | 18h, 24h, or 30h | 24h performance was better than others; SCN lesions did not follow this trend. | (Stephan and Kovacevic, 1978) |
| Passive avoidance | Rat | +12h, +6h, or −6h shifts | 12:12h LD, ZT0.5-2.5 | 48-h or 7 days | Phase-shifted groups had impaired performance. | (Tapp and Holloway, 1981) |
| Passive avoidance | Wistar rat | +4h or −6h shifts | 14:10h LD→DL or DD | 24h, 48h, 96h, 144h | Phase-shifted groups had impaired performance. | (Fekete et al., 1985) |
| Passive avoidance | Wistar rat | −6h shifts; ACTH analog ORG-2766 or DGAVP | 14:10h LD→DL | 24h, 48h,168h | Phase-shifted groups had impaired performance; ACTH and DGAVP attenuated the deficits. | (Fekete et al., 1986) |
| Passive avoidance | Long-Evans rat | ZT time; aging | 12:12h DL, ZT13 or 23 | 24h or 6 weeks | In the early dark phase, performance was better than in the late dark phase tested at 6 weeks, but not 24 h, later in the aged, but not young, group | (Winocur and Hasher, 1999) |
| Fear conditioning | C57BL/6J mouse | ZT time | 12:12h LD; ZT2 or 14 | Every 24-h up to 5 days | Dark phase groups performed better than light ones. | (Valentinuzzi et al., 2001) |
| Fear conditioning (tone-cued) | C-57/6J; C-3H; mouse | ZT time | 12:12h LD or DL or DD, ZT3 or 15 | N.A. | Light phase groups performed better than dark ones. | (Chaudhury and Colwell, 2002) |
| Fear conditioning | C57Bl/6 mouse | ZT time and time cues | 12:12h LD, ZT4-8 or 16-20 (tested at the same or different times) | 24h, 36h, or 48h | ZT4 groups had better performances than others. | (Eckel-Mahan et al., 2008b) |
| Fear conditioning (tone-cued) | Long-Evans rat | Every +3h shift for 6 days(one session) or 4 sessions | 12:12h LD, ZT3 | 24h | No effects of phase shifts. | (Craig and McDonald, 2008) |
| Fear conditioning | C57Bl/6 mouse | Phase shift before or after the LD | 12:12h LD, ZT3 or 6 | 1 to 7days | The phase-shifted group had impaired performance. | (Loh et al., 2010) |
| Fear conditioning | C57Bl/6 mouse | SCN lesions | 12:12h LD | 2weeks | SCN lesions impaired performance. | (Phan et al., 2011) |
| Fear conditioning (extinction) | Sprague-Dawley rat | ZT time | 12:12h LD, ZT4 or 16 | 24h | Facilitated extinction more in the dark phase group than in the light one. | (Woodruff et al., 2015b) |
| Fear conditioning | C57BL/6J mouse | +12h shift or bifurcated 6:6h LD | 12;12h LD, ZT12 or 24 | 12h or 24h | The Phase-shifted group showed impaired retrieval, while the bifurcated group showed impaired learning. | (Harrison et al., 2017) |
| Fear conditioning | C57Bl6/J mouse | ZT time; ITI; Bmal1 deletion | 12:12h LD→DD, CT4 or 16 | 30min, 42h or 54h | The CT4 group had better long-term retrieval than CT16; Bmal1 deletion impaired performance. | (Price and Obrietan, 2018) |
| Fear conditioning (extinction) | Sprague-Dawley rat | ZT time; Per1/2 knockdown in PFC | 12:12h LD, ZT4 or 16 | 24h | Facilitated extinction in the dark phase group; PFC Per1/2 knockdown eliminated this facilitation. | (Woodruff et al., 2018) |
| Fear conditioning (extinction) | C57Bl/6J mouse | +8h shifted across 1 or 2 days | 12:12h LD, ZT13 | 24h or 48h | The phase-shifted group showed impaired fear of extinction. | (Clark et al., 2020) |
| Fear conditioning | Wistar rat | ZT time; DD | 12:12h LD or DD, ZT | The DD group showed facilitated fear extinction, specifically during the light phase. | (Asadian et al., 2022) | |
| Fear conditioning | Siberian hamster | −3 h shift | 16:8h LD, ZT16-20 | 48h | The phase-shifted group showed impaired fear memory. | (Steiger et al., 2022) |
| MWM | Long-Evans rat | +3h shift | 12:12h LD, ZT11 | 2 or 10 days (probe) | There were no effects on learning; the phase-shifted group showed impaired retention. | (Devan et al., 2001) |
| MWM (delayed non-match-to-sample) | Long-Evans rat | ZT time and time cues; aging | 12:12h DL, ZT13 or 23 | 0-80sec | The early dark phase group performed better than the late dark phase group in the old animals, whereas the reverse was true for the young. | (Winocur and Hasher, 2004) |
| MWM | Wistar rat | ZT time | 12:12h LD, ZT3 or 15 | 30 min | Dark phase groups performed better than light ones. | (Valentinuzzi et al., 2004a) |
| MWM | C57BL/6 mouse | LL | 12:12h LD or LL | N.A. (no probe) | The LL group showed impaired learning more than the LD one. | (Fujioka et al., 2011) |
| MWM | Diurnal grass rat | ZT time | 12:12h LD, ZT4 or 16 | 24h | There were no effects on learning; the light phase groups performed better than the dark ones. | (Martin-Fairey and Nunez, 2014a) |
| MWM | ICR mouse | Abnormal LD | 12:12h, 3:5h or 5:3h LD | N.A. | Abnormal LD impaired the performance. | (Li et al., 2017) |
| MWM | Wistar Kyoto and SHR rat | LD disturbance | 12:12h LD, ZT1-2 | 24h (probe) | The LD disturbance impaired the performance. | (Wang et al., 2020) |
| MWM | Wistar rat | LL or DD; fluoxetine | 12:12h LD→ LL or DD, ZT0-3 | 24h | The LL group showed impaired performance, while fluoxetine reversed the deficits. | (Sharma et al., 2021) |
| MWM | Long-Evans rat | 12:9h LD for 6 days | 12:12h LD→12:9h LD, ZT10.5 | 18 days (probe) | The 21-day group showed impaired memory, but not learning. | (Deibel et al., 2022) |
| MWM | Wistar rat | ZT time; DD | 12:12h LD or DD, ZT | The DD group showed impaired spatial memory. | (Asadian et al., 2022) | |
| MWM | Non-Tg and 3xTg-AD mice | ZT time; 3xTg-AD | 12:12h LD, ZT4 or 16 | 24h (probe) | The light group learned faster than the dark one, while the dark group had better reversal learning than the light one. AD impaired probe and reversal memory. | (Carvalho da Silva et al., 2022) |
| NOR | Siberian hamster | ZT time; arrhythmic circadian; PTZ (1 mg/kg, i.p. daily) | 16:8h LD, ZT3, 7, 11, 15, 19, 23 | 60min | Early light groups had impaired performance in controls; the arrhythmic group showed impaired performance; PTZ facilitated performance | (Ruby et al., 2008) |
| NOR | Wistar rat | ZT time | 12:12h LD, ZT2, 12, 14 or 20 | Min or 24h | No effects in time-of-day. | (Takahashi et al., 2013) |
| NOR | Djungarian hamster | ZT time; arrhythmic circadian | 14:10h LD, ZT4, 7, 13, 16, 19 | 1h | ZT13, 16, and 19 groups performed better than ZT4 and 7 groups, and arrhythmic circadian impaired performance. | (Müller et al., 2015) |
| NOR | Djungarian hamster | Arrhythmic circadian | 14:10h LD | 1h | Arrhythmic circadian impaired performance | (Weinert et al., 2016) |
| NOR | C57BL/6 mouse | ZT time; DD; SON lesions | 12:12h LD, ZT0, 4, 8, 12, 16, 20 | 24h | Early light and SCN lesioned groups showed impaired performance. | (Shimizu et al., 2016) |
| NOR & object-displacement recognition | C57BL/6J mouse | ZT time; LL | 12:12h LD, ZT6 or 18; 12:12h LD→LL, CT6 or 18 | 5min or 24h | The light phase group performed better than the dark phase one. | (Tam et al., 2017) |
| NOR | B6/C3H mouse | Ts65Dn; SCN lesions | 12:12h LD, ZT6 | 24h | SCN lesions did not affect memory in controls; Ts65Dn mice had impaired performance, while SCN lesions alleviated it in Ts65Dn mice. | (Chuluun et al., 2020) |
| NOR (one object during the learning and removal in the test) | C57BL/6N Crl mouse | ZT time | 12:12h LD or DD, ZT3.5 or 15.5 | N.A. | The light phase groups performed better than the dark ones in learning, but not memory. | (McCauley et al., 2020) |
| NOR | C57BL/6 mouse | ZT time; dim light (ZT12-16) | 12:12h LD, ZT2 or 14 | 12h | The light phase group performed better than dark phase one; dim light exposure reversed this pattern. | (Tam et al., 2021) |
| NOR | Wistar rat | LL or DD; fluoxetine | 12:12h LD→ LL or DD, ZT0-3 | 24h | The LL group showed impaired memory, while fluoxetine reversed the deficits. | (Sharma et al., 2021) |
| NOR | C57BL/6J mouse | Cry1, Cry2 KO, AAV-Cry1 | 12:12h LD→DD, ZT20-22 | 24h | AAV-Cry1 expression in the SCN attenuated the deficits of Cry1-Cry2 KO. | (Maywood et al., 2021) |
| NOR | C57BL/6 mouse | ZT time | 12:12h LD, ZT0, 6, 12, 18 | 12h or 24h | No effects of time of day (the dark phase groups seemed to perform better in complex object recognition). | (Gessner et al., 2022) |
| NLR | C57BL/6J mouse | ZT time; sex | 12:12h LD→DD, CT4 or 16 | 30min | The dark phase group performed better than the light one in males, while the opposite effect was found in females. | (Goode et al., 2022) |
| Active avoidance | Sprague-Dawley rat | ZT time; ACTH | 12:12h LD, ZT1.5-2.5 or 9-10 | Variable ratio: 90 sec | The late light phase group performed better than the early light phase one; ACTH facilitated performance | (Pagano and Lovely, 1972) |
| Active avoidance (extinction) | Rat | ZT time; ITI | 12:12h LD, ZT0-4, 7-10, 12-15, 18-21 | 15min, 6h, 12h, 18h, 24h | 15min, 12h, and 24h groups had stronger resistance to extinction than the others. | (Holloway and Sturgis, 1976) |
| Active avoidance (extinction) | Rat | ZT time; pinealectomy | 12;12h LD, ZT3 or 15 | 60sec | The dark phase group learned faster than the light one. | (Catalá et al., 1985) |
| Shock avoidance operant task | Sprague-Dawley rat | ZT time | 12:12h LD or DL, ZT2, 6 or 10, 14, 18, 22 | N.A. | Dark phase groups performed better in shock avoidance, but not responses, than light ones. | (Ghiselli and Patton, 1976) |
| CPA (foot shock) | Syrian hamster | ITI | 14:10h LD, | 24, 48, 32, or 40h | 24 and 48h groups were more effective than the 32 and 40h groups. | (Cain et al., 2004a) |
| CPA (foot shock) | Syrian hamster | ZT time and time cues | 14:10h LD, ZT4 or 13 | 24h | Non-matched LD cues impaired performance | (Cain et al., 2008) |
| CPA (foot shock) | Syrian hamster | ZT time and time cues; SCN lesions | 14:10h LD, ZT2 or 11 | 24h | Non-matched LD cues impaired performance: SCN lesions did not affect it. | (Cain et al., 2012) |
| CPP (wheel running) | Syrian hamster | ZT time | 14:10h LD, ZT4 or 13; LL, CT4 or 13 | 24h | The effects were paired with LD cues. | (Ralph et al., 2002) |
| CPP (food) | Rat | Time cue | 12:12h LD, CT2 or 11 (tested at the same or different times) | 24h | No effects of time cues. | (McDonald et al., 2002) |
| CPP (wheel running) | Syrian hamster | ZT time; SCN lesions | 14:10h LD, ZT3 or 14 | 24h | The effects were paired with LD cues, and SCN was not needed. | (Ko et al., 2003) |
| CPP (food) | Wistar and Long-Evans rats | ZT time and time cues | 12:12h LD, ZT3 or 11 (training at ZT11) | 24h | No effects were observed in the Long-Evan rats; non-matched LD cues affected the Wistar rats. | (Cain et al., 2004b) |
| CPP | Syrian hamster | +6h shift every 3 days for 25 days | 14:10h LD, ZT18 | 8 days | The phase-shifted group showed impaired performance. | (Gibson et al., 2010) |
| CPP (food) | Long-Evans rat | Every +3h shift for 6 days→LD 10days, repeated 4 times | 12:12h LD | 24h | The phase-shifted group showed impaired performance. | (McDonald et al., 2013) |
| CPP (morphine) | Wistar rat | ZT time and time cue | 12:12h LD, ZT1-2 or 11-12 | 24h | The late-light phase group showed a stronger preference than the early-light ones. | (Khaksari et al., 2022) |
| Radial-arm maze | Sprague-Dawley rat | DL; theophylline (15mg/kg, i.p. daily) | 12:12h LD or DL | 7 or 14 days | The dark phase group performed better than the light one; theophylline facilitated performance only in the light phase. | (Hauber and Bareiß, 2001) |
| Radial-arm maze | C3H/HeN mouse | ZT time; Per1 depletion | 12:12h LD, ZT2 or 14 | 24h | The light phase group performed better than the dark ones; Per1 depletion reversed this pattern. | (Rawashdeh et al., 2014) |
| T-maze operant task | Wistar rat | ZT time; SCN ablation | 12:12h LD→DD, ZT3-4, or 10-11 | Variable ratio 10 sec | Intact learning without LD cues and SCN. | (Mistlberger et al., 1996) |
| Spontaneous T-maze | Siberian hamster | ZT time; arrhythmic circadian; PTZ (0.3 or 1 mg/kg, i.p. daily) | 16:8h LD, ZT3, 7, 11, 15, 19, 23 | N.A. | Late light and dark phase groups performed better than early light ones; PTZ improved performanc e in the arrhythmic circadian group. | (Ruby et al., 2013) |
| Spontaneous T-maze | Siberian hamster | Arrhythmic circadian; SCN lesions | 16:8h LD, | N.A. | Arrhythmic circadian lesions, but not SCN lesions, impaired performance. | (Fernandez et al., 2014) |
| Spontaneous T-maze | C57BL/6J mouse | ZT time; diet | 12:12h LD, ZT2 or 14 | N.A. | The dark phase group performed better than the light one; high fat and sucrose diets impaired it. | (Davis et al., 2020) |
| Spontaneous T-maze | C57BL/6J mouse | ZT time; diet | 12:12h LD, ZT2 or 14 | N.A. | The dark phase group performed better than the light one; a high-fat diet impaired it. | (Davis et al., 2021) |
| Spontaneous T-maze | C57BL/6J mouse | ZT time; diet | 12:12h LD, ZT2 or 14 | N.A. | The dark phase group performed better than the light one; a high-fat diet impaired it. | (Davis et al., 2021) |
| Spontaneous Y-maze | Wistar rat | LL or DD; fluoxetine | 12:12h LD→ LL or DD, ZT0-3 | N.A. | LL group showed impaired memory, while fluoxetine reversed the deficits. | (Sharma et al., 2021) |
| Spontaneous T-maze | C57BL/6J mouse | ZT time; Tg-SwDI | 12:12h LD, ZT2 or 14 | N.A. | The dark phase group performed better than the light one; the Tg-SwDI mouse had impaired performance. | (Fusilier et al., 2021) |
| 6-point alley T-maze | C57Bl/6 mouse | ZT time | 12:12h LD, ZT2, 6, 10, 14, 18, 22 | N.A. | Dark phase groups performed better than light ones. | (Hoffmann and Balschun, 1992) |
| Spontaneous Y-maze | C57BL/6J mouse | SCN lesions | 12:12h LD | N.A. | SCN lesions did not affect performance. | (Mulder et al., 2014) |
| Sustained attention operant task | Sprague-Dawley rat | ZT time | 12:12h LD, ZT4 or 16 | N.A. | The dark phase group performed better than the light one. | (Gritton et al., 2012b) |
| Sustained attention operant task | Sprague-Dawley rat | ZT time; SCN lesions | 12:12h LD, ZT 4 or 16 | N.A. | The dark phase group performed better than the light one; SCN lesions impaired performance at ZT4. | (Gritton et al., 2013) |
| Barnes maze | Mouse | ZT time; Bmal1 forebrain deletion | 12:12h LD, ZT4 or 16 | 17days (probe) | Bmal1 deletion led to learning and recall deficits at both times. | (Price et al., 2016) |
| Barnes maze | C57BL/6J mouse | ZT time; elF4E or MNK depletion | 12:12h LD, ZT6 or 18 | 24h (probe) | Dark phase groups performed better than light ones; elF4E and MNK depletions affected learning but not memory. | (Liu et al., 2022) |
| Social recognition | Djungarian hamster | Arrhythmic circadian; social ranking | 14:10h LD | 2min or 24h | The social subordinate, but not dominant, animals had intact 24-h memory; arrhythmic circadian impairment impaired the memory | (Weinert et al., 2016) |
| Social recognition | C57BL/6N mouse | ZT time; time cues; Bmal1 deletion | 12:12h LD, ZT4 or 10 | 6h or 24h | ZT10 showed impaired retrieval of weak social memory in WT; Bmal1 deletion impaired memory at both times. | (Hasegawa et al., 2019) |
| Licking latency task | Rat | ITI | 12:12h LD, ZT1.5-4 or 5.5-8 | 15min, 1-h or every 6h up to 36h | 12h, 24h, and 36h groups performed better than others. | (Wansley and Holloway, 1975) |
| Circadian time-place three-arms task | C57BL/6J mouse | ZT time; Cry depletion | 12:12h LD, ZT2-3.5, 5-6.5 or 8-9.5 | 3h | Animals were able to learn specific time-place rules, but the Cry gene knockout impaired it. | (Van der Zee et al., 2008) |
Abbreviations: ZT: zeitgeber time; CT: circadian time; LD or DL: light-dark cycle; DD: dark-dark cycle; MWM: Morris water maze; N.A. not applicable or within seconds; CTA: conditioned taste aversion; CPP: conditioned place preference; CPA: conditioned place avoidance; ACTH: adrenocorticotropic hormone; DGAVP: desglycinamide−9-(Arg8)-vasopressin; PTZ: pentylenetetrazol; SHR: spontaneously hypertensive rat; PFC; prefrontal cortex; Tg-SwDI: the human APP gene with K670N/M671L, E693Q and D694N mutations; 3xTg AD: the TauP301L, APPSwe, and γ-secretase (PS1M146V); NOR, novel object recognition with 24 h training-testing interval; TMh, time memory to heat exposure; cTPL, circadian time place memory; CFC, contextual fear conditioning; NLR, novel location recognition; CR, conditioned reflex; Ts65Dn: segmental trisomic 16 on the B6/C3h background