Fasting Launches CRTC to Facilitate Long-Term Memory Formation in
            <i>Drosophila</i>

Hirano, Yukinori; Masuda, Tomoko; Naganos, Shintaro; Matsuno, Motomi; Ueno, Kohei; Miyashita, Tomoyuki; Horiuchi, Junjiro; Saitoe, Minoru

doi:10.1126/science.1227170

Cited by 115 publications

(117 citation statements)

References 35 publications

Supporting

Mentioning

113

Contrasting

Order By: Relevance

“…It has been reported that appetitive long-term memory (LTM) is consolidated more quickly than aversive LTM [36,37]. Moreover, Hirano et al showed that different LTM systems are utilized in the hungry state [38]. The rats used for MAZE testing in this study were kept at a mildly hungry state, thus different effects from GEN exposure may have occurred.…”

Section: Discussionmentioning

confidence: 99%

Perinatal exposure to genistein, a soy phytoestrogen, improves spatial learning and memory but impairs passive avoidance learning and memory in offspring

Kohara

Kuwahara

Kawaguchi

et al. 2014

Physiology & Behavior

View full text Add to dashboard Cite

This study investigated the effects of perinatal genistein (GEN) exposure on the central nervous system of rat offspring. Pregnant dams orally received GEN (1 or 10 mg/kg/day) or vehicle (1 ml/kg/day) from gestation day 10 to postnatal day 14. In order to assess the effects of GEN on rat offspring, we used a battery of behavioral tests, including the open-field, elevated plus-maze, MAZE and step-through passive avoidance tests. MAZE test is an appetite-motivation test, and we used this mainly for assessing spatial learning and memory. In the MAZE test, GEN groups exhibited shorter latency from start to goal than the vehicle-treated group in both sexes. On the other hand, performances in the step-through passive avoidance test were non-monotonically inhibited by GEN in both sexes, and a significant difference was observed in low dose of the GEN-treated group compared to the vehicle-treated group in female rats. Furthermore, we found that perinatal exposure to GEN did not significantly alter locomotor activity or emotionality assessed by the open-field and elevated-plus maze tests. These results suggest that perinatal exposure to GEN improved spatial learning and memory of rat offspring, but impaired their passive avoidance learning and memory.

show abstract

Section: Discussionmentioning

confidence: 99%

Perinatal exposure to genistein, a soy phytoestrogen, improves spatial learning and memory but impairs passive avoidance learning and memory in offspring

Kohara

Kuwahara

Kawaguchi

et al. 2014

Physiology & Behavior

View full text Add to dashboard Cite

show abstract

“…Many molecules that are specifically required for LTM have been identified, and some of these molecules are involved in learning-dependent gene transcription/ translation (3,(53)(54)(55)(56)(57). For instance, fasting-dependent LTM that is formed without training repetition requires CREB-regulated transcription coactivator (CRTC)-mediated cAMP response element binding protein (CREB) transcription in the MB (12). Such a transcription-dependent mechanism takes time and may thus underlie gradual formation of memory induced by the ltm-PAM.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have revealed aspects of the molecular and cellular mechanisms of LTM formation induced by repetitive training (8)(9)(10)(11), but how a single training induces a stable LTM is poorly understood (12).…”

mentioning

confidence: 99%

Distinct dopamine neurons mediate reward signals for short- and long-term memories

Yamagata

Ichinose

Aso

et al. 2014

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

221

287

View full text Add to dashboard Cite

Drosophila melanogaster can acquire a stable appetitive olfactory memory when the presentation of a sugar reward and an odor are paired. However, the neuronal mechanisms by which a single training induces long-term memory are poorly understood. Here we show that two distinct subsets of dopamine neurons in the fly brain signal reward for short-term (STM) and long-term memories (LTM). One subset induces memory that decays within several hours, whereas the other induces memory that gradually develops after training. They convey reward signals to spatially segregated synaptic domains of the mushroom body (MB), a potential site for convergence. Furthermore, we identified a single type of dopamine neuron that conveys the reward signal to restricted subdomains of the mushroom body lobes and induces long-term memory. Constant appetitive memory retention after a single training session thus comprises two memory components triggered by distinct dopamine neurons.dopamine | learning and memory | Drosophila | mushroom body M emory of a momentous event persists for a long time.Whereas some forms of long-term memory (LTM) require repetitive training (1-3), a highly relevant stimulus such as food or poison is sufficient to induce LTM in a single training session (4-7). Recent studies have revealed aspects of the molecular and cellular mechanisms of LTM formation induced by repetitive training (8-11), but how a single training induces a stable LTM is poorly understood (12).Appetitive olfactory learning in fruit flies is suited to address the question, as a presentation of a sugar reward paired with odor induces robust short-term memory (STM) and LTM (6, 7). Odor is represented by a sparse ensemble of the 2,000 intrinsic neurons, the Kenyon cells (13). A current working model suggests that concomitant reward signals from sugar ingestion cause associative plasticity in Kenyon cells that might underlie memory formation (14-20). A single activation session of a specific cluster of dopamine neurons (PAM neurons) by sugar ingestion can induce appetitive memory that is stable over 24 h (19), underscoring the importance of sugar reward to the fly.The mushroom body (MB) is composed of the three different cell types, α/β, α′/β′, and γ, which have distinct roles in different phases of appetitive memories (11,(21)(22)(23)(24)(25). Similar to midbrain dopamine neurons in mammals (26,27), the structure and function of PAM cluster neurons are heterogeneous, and distinct dopamine neurons intersect unique segments of the MB lobes (19,(28)(29)(30)(31)(32)(33)(34). Further circuit dissection is thus crucial to identify candidate synapses that undergo associative modulation.By activating distinct subsets of PAM neurons for reward signaling, we found that short-and long-term memories are independently formed by two complementary subsets of PAM cluster dopamine neurons. Conditioning flies with nutritious and nonnutritious sugars revealed that the two subsets could represent different reinforcing properties: sweet taste and nutritional value of sugar....

show abstract

“…The exposure of flies to repetitive training cycles with gaps between the training cycles (spaced training) leads to a consolidated form of long-term memory that is CREB transcription dependent and lasts up to a week. Training without gaps (massed training) leads to the formation of anesthesia-resistant memory (ARM), which similar to long-term memory, is typically measured 24 hr after 5 cycles of training 7,13,[15][16][17]20,21 .…”

Section: Introductionmentioning

confidence: 99%

“…The length of the adult stage accommodates longer-term genetic, behavioral, dietary and pharmacological manipulations of memory, in addition to determining the effect of aging and neurodegenerative disease on memory [3][4][5][6][11][12][13][15][16][17][18][19][20][21] . Classical conditioning is induced by the simultaneous presentation of a neutral odor cue (conditioned stimulus, CS + ) and a reinforcement stimulus, e.g., an electric shock or sucrose, (unconditioned stimulus, US), that become associated with one another by the animal 1,16 .…”

mentioning

confidence: 99%