Circadian modulation of memory and plasticity gene products in a diurnal species

Abstract

Cognition is modulated by circadian rhythms, in both nocturnal and diurnal species. Rhythms of clock gene expression occur in brain regions that are outside the master circadian oscillator of the suprachiasmatic nucleus and that control cognitive functions, perhaps by regulating the expression neural-plasticity genes such as brain derived neurotrophic factor (BDNF) and its high affinity receptor, tyrosine kinase B (TrkB). In the diurnal grass rat (Arvicanthis niloticus), the hippocampus shows rhythms of clock genes that are 180° out of phase with those of nocturnal rodents. Here, we examined the hypothesis that this reversal extends to the optimal phase for learning a hippocampal-dependent task and to the phase of hippocampal rhythms in BDNF/TrkB expression. We used the Morris water maze (MWM) to test for time of day differences in reference memory and monitored daily patterns of hippocampal BDNF/TrkB expression in grass rats. Grass rats showed superior long-term retention of the MWM, when the training and testing occurred during the day as compared to the night, at a time when nocturnal laboratory rats show superior retention; acquisition of the MWM was not affected by time of day. BDNF/TrkB expression was rhythmic in the hippocampus of grass rats, and the phase of the rhythms was reversed compared to that of nocturnal rodents. Our findings provide correlational evidence for the claim that the circadian regulation of cognition may involve rhythms of BDNF/TrkB expression in the hippocampus and that their phase may contribute to species differences in the optimal phase for learning.

Modulation of learning and memory by the targeted deletion of the circadian clock gene Bmal1 in forebrain circuits

“…After acquisition, mice were maintained in their home cages for 17 days (in order to test for long-term memory similarly to Ref. [33]). On day 21, mice were returned to the maze for a 90-s probe trial (as utilized in Ref.…”

The primate seahorse rhythm

“…The circadian system can also influence the acquisition and recall of learned behaviors (Chaudhury and Colwell, 2002;Eckel-Mahan et al, 2008;Fernandez et al, 2003;Lyons et al, 2006) both in rodents (Chaudhury and Colwell, 2002;Hauber and Bareiss, 2001;Lyons et al, 2005) and humans, in which time of day influences memory (Maury and Queinnec, 1992;Nesca and Koulack, 1994). These observations suggest a fundamental interaction between the functions and processing of the hippocampus and the circadian system (Hauber and Bareiss, 2001;Martin-Fairey and Nunez, 2014;Nesca and Koulack, 1994;Smarr et al, 2014).…”

“…This is reflected in behaviors such as sleep-wake behavior, body temperature, the regulation of hormone secretion, and the acquisition and processing of memory (Chaudhury and Colwell, 2002;Gerstner et al, 2009;Nesca and Koulack, 1994;Ruby et al, 2008Ruby et al, , 2013. Different models in rodents and humans have highlighted remarkable changes in cognitive functions, memory acquisition and recall across the day as well as the circadian modulation of neurogenesis, synaptic remodeling, intracellular cascades, and the epigenetic regulation of gene expression (Hauber and Bareiss, 2001;Martin-Fairey and Nunez, 2014;Smarr et al, 2014). Furthermore, functions such as processing and learning in the hippocampal memory have been described as important to integrate the circadian information of independent oscillators (Garren et al, 2013;Maury and Queinnec, 1992;Nesca and Koulack, 1994;Smarr et al, 2014).…”

Synchrony and desynchrony in circadian clocks: impacts on learning and memory

“…In molluscan models, peak memory formation for intermediate and longterm memory occurs in phase with the animal's activity period (Fernandez et al 2003;Wagatsuma et al 2004;Lyons et al 2005Lyons et al , 2008Michel et al 2013). Similarly in rodents, peak performance in the Morris water maze for the diurnal grass rat occurs during the day, while peak performance at night is observed for nocturnal animals (Valentinuzzi et al 2004;Martin-Fairey and Nunez 2014). However, core circadian gene expression in the SCN appears similarly phased in nocturnal and diurnal rodent species, suggesting that the contrasting phases of memory formation are regulated downstream from the master circadian clock.…”

“…However, core circadian gene expression in the SCN appears similarly phased in nocturnal and diurnal rodent species, suggesting that the contrasting phases of memory formation are regulated downstream from the master circadian clock. Neurons of the hippocampus and the amygdala exhibit rhythms in core circadian gene expression (Lamont et al 2005;Wang et al 2009;Li et al 2013) with the hippocampal circadian gene expression anti-phasic for the diurnal grass rat and nocturnal rodents (Ramanathan et al 2010;Martin-Fairey and Nunez 2014). Phase differences in gene expression also occur in brain regions downstream from the SCN for diurnal versus nocturnal Degus (Otalora et al 2013).…”