Light modulates hippocampal function and spatial learning in a diurnal rodent species: A study using male nile grass rat (<i>Arvicanthis niloticus</i>)

Soler, Joel E.; Robison, Alfred J.; Núñez, Antonio A.; Yan, Lili

doi:10.1002/hipo.22822

Cited by 39 publications

(41 citation statements)

References 104 publications

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“…If environmental light, which is available daily to all animals in nature, can be used for transcriptional activation in the brain, such a light-driven transcription system is considered reasonable and effective for continually providing de novo protein synthesis required for LTM maintenance. When diurnal Nile grass rats were housed under dim LD cycles, 24 h spatial memory was impaired, and this lighting condition inhibited the expression of brain-derived neurotrophic factors and the dendritic spine density in the hippocampus (Soler et al, 2018). Although it is not clarified whether the rapid forgetting in the Nile grass rats under dim LD cycles results from the inhibition of de novo protein synthesis required for LTM maintenance, lightdependent de novo protein synthesis in the memory center may be conserved in many animal species.…”

Section: Discussionmentioning

confidence: 99%

Environmental Light Is Required for Maintenance of Long-Term Memory inDrosophila

et al. 2020

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Long-term memory (LTM) is stored as functional modifications of relevant neural circuits in the brain. A large body of evidence indicates that the initial establishment of such modifications through the process known as memory consolidation requires learning-dependent transcriptional activation and de novo protein synthesis. However, it remains poorly understood how the consolidated memory is maintained for a long period in the brain, despite constant turnover of molecular substrates. Using the Drosophila courtship conditioning assay of adult males as a memory paradigm, here, we show that in Drosophila, environmental light plays a critical role in LTM maintenance. LTM is impaired when flies are kept in constant darkness (DD) during the memory maintenance phase. Because light activates the brain neurons expressing the neuropeptide pigment-dispersing factor (Pdf), we examined the possible involvement of Pdf neurons in LTM maintenance. Temporal activation of Pdf neurons compensated for the DD-dependent LTM impairment, whereas temporal knockdown of Pdf during the memory maintenance phase impaired LTM in light/dark cycles. Furthermore, we demonstrated that the transcription factor cAMP response element-binding protein (CREB) is required in the memory center, namely, the mushroom bodies (MBs), for LTM maintenance, and Pdf signaling regulates light-dependent transcription via CREB. Our results demonstrate for the first time that universally available environmental light plays a critical role in LTM maintenance by activating the evolutionarily conserved memory modulator CREB in MBs via the Pdf signaling pathway.

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Section: Discussionmentioning

confidence: 99%

Environmental Light Is Required for Maintenance of Long-Term Memory inDrosophila

et al. 2020

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“…If environmental light, which is available daily to all animals in nature, can be used for transcriptional activation in the brain, such a light-driven transcription system is considered reasonable and effective for continually providing de novo protein synthesis required for LTM maintenance. When diurnal Nile grass rats were housed under dim LD cycles, 24 h spatial memory is impaired, and this lighting condition inhibits the expression of brain-derived neurotrophic factors and dendritic spine density in the hippocampus (Soler et al, 2018). Although it is unknown whether the rapid forgetting in the Nile grass rats under dim LD cycles results from the inhibition of de novo protein synthesis required for LTM maintenance, light-dependent de novo protein synthesis in the memory center may be conserved in many animal species.…”

Section: Discussionmentioning

confidence: 99%

Environmental light is required for maintenance of long-term memory in Drosophila

Inami

Sato

Kondo³

et al. 2019

Preprint

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17 18 Long-term memory (LTM) is stored as functional modifications of relevant neural circuits 19 in the brain. However, it remains poorly understood how the consolidated memory is 20 maintained for a long period. Here, we show that in Drosophila, universally available 21 environmental light plays a critical role in LTM maintenance by reactivating the memory 22 modulator cAMP response element-binding protein (CREB) via neuropeptide signaling. 23 LTM is impaired when flies are kept in constant darkness during the memory maintenance 24 phase. Because light activates the brain neurons expressing the neuropeptide 25 Pigment-dispersing factor (Pdf) through the brain photoreceptors, we examined the 26 possible involvement of Pdf in LTM maintenance and found that temporal knockdown of 27 Pdf during the memory maintenance phase impairs LTM in light-dark cycles. Furthermore, 28 we demonstrated that the Pdf receptor (Pdfr) and CREB are required in the memory center 29 for LTM maintenance and Pdfr regulates light-dependent transcription via CREB.30 3 90When flies were kept in LL after conditioning, their LTM was intact [ Figure 1A; (7)], as previously 91 reported (Sakai et al., 2004). Furthermore, the LTM of several clock mutants except for period (per) 92 5 mutants is intact (Sakai et al., 2004). Thus, light input, but not the circadian clock, is necessary for LTM 93 maintenance. 94 Sleep plays an important role in the consolidation of Drosophila courtship memory (Donlea et al., 95 2011). However, it remains unclear whether an abnormal sleep phenotype is attributable to disturbed 96 LTM maintenance of flies kept in DD. To examine whether light conditions affect Drosophila sleep (see 97 Materials and methods), sleep amount was measured in flies kept in LD and DD (Figure 2A). The mean 98 amount of daytime sleep of flies kept in DD was lower than that of flies kept in LD (Figures 2A-C).99 However, when flies in LD were slightly deprived of sleep to adjust the amount of daytime sleep to the 100 level of that in DD (Figures 2D-F), their LTM maintenance was not attenuated (Figure 2G). Thus, LTM 101 impairment induced by DD does not simply result from the reduced amount of sleep. 102 103 Expression of brain photoreceptors in Pdf neurons is necessary for LTM maintenance in LD 104 Because light directly activates Pdf neurons through circadian photoreceptors [Rhodopsin 7 (Rh7) and 105 Cryptochrome (Cry)] (Fogle et al., 2011; Ni et al., 2017; Sheeba et al., 2008), Pdf neurons may regulate 106 light-driven LTM maintenance. To examine whether Rh7 and Cry are required for LTM, Rh7 and cry null 107 mutant flies (Rh7 1 and cry 01 , respectively) were used. Since memory on d 1 (one day after conditioning) 108 was intact in Rh7 1 and cry 01 flies after 7 h conditioning (Figure 1B), Rh7 and cry are dispensable for 109 memory consolidation. Unlike the memory on d 1, Rh7 1 and cry 01 flies showed memory impairment on d 110 5 ( Figure 1C), suggesting that Rh7 and Cry are required for keeping LTM more than one day. We next 111 sought to determin...

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“…Neuroplasticity acts as a reorganizer in response to insults, resulting in the spontaneous recovery from neuronal damage and functional deficits [3]. BDNF expression, however, is correlated with cognitive recovery in a TBI model [29], and SYP is involved in vesicular trafficking, docking, synaptogenesis, synaptic reorganization, and fusion of the synaptic plasma membrane. SYP can be also used to measure quantitative synaptic remodeling with reference to the formation of new synapses [30].…”

Section: Discussionmentioning

confidence: 99%

Icariin Improves Functional Behavior in a Mouse Model of Traumatic Brain Injury and Promotes Synaptic Plasticity Markers

et al. 2018

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Epimedii Herba (EH) has been used in traditional Asian medicine to treat hemiplegia following stroke. Icariin, its major active component, is used as a quality-control marker and for its various pharmacological effects. We hypothesized that icariin would show protective effects following traumatic brain injury (TBI). The TBI mouse model was induced using a controlled cortical impact method. Body weight, brain damage, motor function, and cognitive function were evaluated. Synaptogenesis markers were analyzed to investigate potential mechanisms of action. The animals were divided into six groups: sham, control, minocycline-treated group, and icariin-treated (3, 10, and 30 mg/kg, p. o.) groups. The icariin 30 mg/kg-treated group regained body weight at 7 and 8 d post TBI. Icariin 30 mg/kg- and 10 mg/kg-treated groups showed enhanced sensory-motor function at 8 d post TBI in rotarod and balance beam tests. Icariin-treated groups showed increased recognition index in the novel object recognition test at all doses and increased spontaneous alternation in the Y-maze test at 30 mg/kg. Icariin upregulated brain-derived neurotrophic factor, synaptophysin and postsynaptic density protein 95 expressions. However, no protective effects against brain damage or neuronal death were observed. The current results provide a basis for using icariin following TBI and suggest that it could be a candidate for the development of therapeutic agents for functional recovery after TBI.

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Light modulates hippocampal function and spatial learning in a diurnal rodent species: A study using male nile grass rat (Arvicanthis niloticus)

Cited by 39 publications

References 104 publications

Environmental Light Is Required for Maintenance of Long-Term Memory inDrosophila

Environmental Light Is Required for Maintenance of Long-Term Memory inDrosophila

Environmental light is required for maintenance of long-term memory in Drosophila

Icariin Improves Functional Behavior in a Mouse Model of Traumatic Brain Injury and Promotes Synaptic Plasticity Markers

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