Effect of circadian phase on context and cued fear conditioning in C57BL/6J mice

Valentinuzzi, Verónica Sandra; Kolker, Daniel E.; Vitaterna, Martha Hotz; Ferrari, E; Takahashi, Joseph S.; Turek, Fred W.

doi:10.3758/bf03192822

Cited by 58 publications

(64 citation statements)

References 41 publications

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“…Some studies in mammals have suggested circadian modulation of learning (6,8,9). LTS demonstrated both diurnal and circadian rhythms in Aplysia (Figs.…”

Section: Discussionmentioning

confidence: 99%

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Circadian modulation of long-term sensitization in Aplysia

Fernandez

Lyons

Levenson

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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As the mechanisms for learning and memory are elucidated, modulation of learning and memory becomes a central issue. We studied the modulation of learning and memory by investigating the circadian regulation of short-and long-term sensitization of the siphon withdrawal reflex in Aplysia. We found that Aplysia exhibited diurnal and circadian rhythms of long-term sensitization (LTS) with significantly greater LTS occurring when animals were trained and tested during the day relative to those trained and tested at night. In contrast to the modulation of LTS, short-term sensitization was not regulated by the circadian clock. Time of training rather than time of testing determined the circadian rhythm of LTS. Animals trained during the subjective day demonstrated LTS when tested during either the day or the night. Conversely, when animals were trained during the night, LTS was not observed when animals were tested either at night or during the day. Thus, the circadian rhythm of LTS is a rhythm in learning rather than a rhythm in recall. The threshold required to elicit siphon withdrawal and the duration of siphon withdrawal were not regulated by the circadian clock. These results indicate that the circadian oscillator exerts strong modulatory influences on one form of long-term memory in Aplysia.H ow organisms learn has been of interest for centuries as people seek to understand and improve learning and memory abilities. One aspect of understanding learning and memory is determining how these processes are normally modulated. What conditions modulate learning and memory, and how does regulation occur? General health, motivation, age, stress, sleep patterns, and time of day may modulate learning and memory. The circadian clock regulates many behavioral and physiological processes, making it likely that circadian modulation of learning and memory also occurs (1).Circadian modulation of learning and memory has been investigated with varied results. Some studies have indicated time of day influences memory in humans (2-4), whereas other studies have found little impact of time of day on memory (5). Researchers studying hippocampus-dependent learning found that rats trained at midday showed decreased retention compared with animals trained earlier or later (6). However, other researchers found no time-of-day effects on multiple learning tasks (7). Furthermore, two laboratories studying contextual fear conditioning in mice reported different effects of the circadian clock on learning and memory (8, 9). The issue of circadian modulation of learning and memory remains to be determined.Indirect evidence for circadian modulation of learning and memory comes from in vitro studies of long-term potentiation. Researchers have documented diurnal and circadian differences in long-term potentiation in the hippocampus (10, 11). Additional studies have also found that excitability of CA3 neurons is regulated diurnally (12). Thus, some mechanisms exist for learning and memory to be rhythmic. Experiments demonstrating that consolidation ...

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“…Some studies in mammals have suggested circadian modulation of learning (6,8,9). LTS demonstrated both diurnal and circadian rhythms in Aplysia (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…However, other researchers found no time-of-day effects on multiple learning tasks (7). Furthermore, two laboratories studying contextual fear conditioning in mice reported different effects of the circadian clock on learning and memory (8,9). The issue of circadian modulation of learning and memory remains to be determined.…”

mentioning

confidence: 99%

Circadian modulation of long-term sensitization in Aplysia

Fernandez

Lyons

Levenson

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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“…31). Owing to previous reports of a circadian modulation on fear conditioning (32,33), preexposure, conditioning, and testing were all performed between ZT7 and ZT12.…”

Section: Methodsmentioning

confidence: 99%

Light enhances learned fear

Warthen¹,

Wiltgen

Provencio³

2011

Proc. Natl. Acad. Sci. U.S.A.

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The ability to learn, remember, and respond to emotional events is a powerful survival strategy. However, dysregulated behavioral and physiological responses to these memories are maladaptive. To fully understand learned fear and the pathologies that arise during response malfunction we must reveal the environmental variables that influence learned fear responses. Light, a ubiquitous environmental feature, modulates cognition and anxiety. We hypothesized that light modulates responses to learned fear. Using tone-cued fear conditioning, we found that light enhances behavioral responses to learned fear in C57BL/6J mice. Mice in light freeze more in response to a conditioned cue than mice in darkness. The absence of significant freezing during a 2-wk habituation period and during intertrial intervals indicated that light specifically modulates freezing to the learned acoustic cue rather than the context of the experimental chamber. Repeating our assay in two photoreceptor mutant models, Pde6b rd1/rd1 and Opn4 −/− mice, revealed that lightdependent enhancement of conditioned fear is driven primarily by the rods and/or cones. By repeating our protocol with an altered lighting regimen, we found that lighting conditions acutely modulate responses when altered between conditioning and testing. This is manifested either as an enhancement of freezing when light is added during testing or as a depression of freezing when light is removed during testing. Acute enhancement, but not depression, requires both rod/cone-and melanopsin-dependent photoreception. Our results demonstrate a modulation by light of behavioral responses to learned fear.L ight is a pervasive feature of the environment and exerts broad effects on behavior and physiology via two parallel pathways (1). The familiar image-forming visual pathway allows discernment of objects in the environment according to physical qualities: their color, form, texture, and motion. The parallel non-image forming (NIF) pathway enables light to exert numerous effects on physiology and behavior independently of image formation, such as pupil constriction, modulation of heart rate, and the synchronization of circadian rhythms and sleepwake cycles to the daily light-dark cycle (2). In addition to the effects of light on basic physiological functions, light also modulates higher-order cognitive processes, including anxiety, mood, and alertness/awakeness (3, 4). The retina, the sole photosensory organ in mammals, projects directly to brain regions involved in emotional responses. Among these are the amygdala, the bed nucleus of the stria terminalis, and the periaqueductal gray (5). Activity in some of these regions is known to be acutely modulated by light in a wavelength-dependent manner (3, 6), whereas the link between photoreception and function in other retinorecipient emotional processing areas remains to be elucidated.Brain sites involved in emotional processing participate in the critical function of learning and remembering emotionally arousing events. This function enables ...

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“…Other, more sensitive measures may be needed to differentiate between the two possibilities. Previous studies have found that while circadian phase affects training and retrieval of contextual fear in C57BL/6 mice, tone memory appears to be independent of circadian phase in some [42], but not all [15], circadian perturbation paradigms. Therefore, it is probable that the deficit for retrieval of cued memory seen in the Advancing group is a direct consequence of circadian disruption, rather than an effect of testing at a non-comparable phase.…”

Section: Bifurcation Does Not Disrupt Long-term Memory To the Extent mentioning

confidence: 99%

“…These differences may be attributable to differences in strain, fear conditioning protocol (i.e., time between context and tone tests; the number, timing, or voltage of shocks), or to the fact that our mice had access to running wheels. In a report by Valentinuzzi and colleagues [42] wherein phase of fear conditioning was examined in C57BL/6J mice with access to running wheels, animals trained and tested early in subjective night, rather than day, showed higher rates of freezing to context 24 h post-training. In rats, performance on a novel location recognition task, which like the context test in our paradigm is hippocampal-dependent, likewise peaked at night rather than day [43].…”

Section: Phase Effects Are Found For Control But Not Bifurcated Micementioning

confidence: 99%

Circadian waveform bifurcation, but not phase-shifting, leaves cued fear memory intact

Harrison

Carmack

Block

et al. 2017

Physiology & Behavior

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• The circadian system was experimentally bifurcated into two days and nights per 24 h.• Pavlovian fear conditioning was used to quantify acquisition and retrieval of memory.• Retrieval of cued fear remained intact in bifurcated, but not phase-shifted, mice. a b s t r a c t a r t i c l e i n f o In mammals, memory acquisition and retrieval can be affected by time of day, as well as by manipulations of the light/dark cycle. Under bifurcation, a manipulation of circadian waveform, two subjective days and nights are experimentally induced in rodents. We examined the effect of bifurcation on Pavlovian fear conditioning, a prominent model of learning and memory. Here we demonstrate that bifurcation of the circadian waveform produces a small deficit in acquisition, but not on retrieval of fear memory. In contrast, repeated phase-shifting in a simulated jet-lag protocol impairs retrieval of memory for cued fear. The results have implications for those attempting to adjust to shift-work or other challenging schedules.

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Effect of circadian phase on context and cued fear conditioning in C57BL/6J mice

Cited by 58 publications

References 41 publications

Circadian modulation of long-term sensitization in Aplysia

Circadian modulation of long-term sensitization in Aplysia

Light enhances learned fear

Circadian waveform bifurcation, but not phase-shifting, leaves cued fear memory intact

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