Training with inedible food in <i>Aplysia</i> causes expression of C/EBP in the buccal but not cerebral ganglion

Levitan, David; Lyons, Lisa C.; Perelman, Alexander; Green, Charity L.; Motro, Benny; Eskin, Arnold; Susswein, Abraham J.

doi:10.1101/lm.970408

Cited by 23 publications

(47 citation statements)

References 51 publications

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“…[45][46][47][48] In Aplysia, gene expression and protein synthesis after training are necessary for long-term LFI memory. 32,49,50 To determine whether the effect of sleep deprivation on the consolidation of memory is phylogenetically conserved, animals were trained at ZT 11 during the late day, sleep deprived for the first 9 h of the night (ZT 12-ZT 21), and then tested for LTM 24 h after training. Sleep deprivation after training impaired LTM as sleep deprived animals had response times significantly greater than non-sleep deprived control animals ( Figure 2A; Figure S1C).…”

Section: Sleep Deprivation Blocks the Consolidation Of Ltmmentioning

confidence: 99%

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Krishnan

Gandour

Ramos

et al. 2016

Sleep

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Study Objectives: Insufficient sleep in individuals appears increasingly common due to the demands of modern work schedules and technology use. Consequently, there is a growing need to understand the interactions between sleep deprivation and memory. The current study determined the effects of acute sleep deprivation on short and long-term associative memory using the marine mollusk Aplysia californica, a relatively simple model system well known for studies of learning and memory. Methods: Aplysia were sleep deprived for 9 hours using context changes and tactile stimulation either prior to or after training for the operant learning paradigm, learning that food is inedible (LFI). The effects of sleep deprivation on short-term (STM) and long-term memory (LTM) were assessed. Results: Acute sleep deprivation prior to LFI training impaired the induction of STM and LTM with persistent effects lasting at least 24 h. Sleep deprivation immediately after training blocked the consolidation of LTM. However, sleep deprivation following the period of molecular consolidation did not affect memory recall. Memory impairments were independent of handling-induced stress, as daytime handled control animals demonstrated no memory deficits. Additional training immediately after sleep deprivation failed to rescue the induction of memory, but additional training alleviated the persistent impairment in memory induction when training occurred 24 h following sleep deprivation. Conclusions: Acute sleep deprivation inhibited the induction and consolidation, but not the recall of memory. These behavioral studies establish Aplysia as an effective model system for studying the interactions between sleep and memory formation.

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Section: Sleep Deprivation Blocks the Consolidation Of Ltmmentioning

confidence: 99%

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Krishnan

Gandour

Ramos

et al. 2016

Sleep

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“…We have reported that, after training with inedible food, ApC/EBP is transcribed and translated in the buccal ganglia (Levitan et al 2008). A subsequent study also localized the expression of MAP kinase after training to the buccal ganglia (Michel et al 2011).…”

Section: Apc/ebp Expression Is Present In Mechanoafferent Neuronsmentioning

confidence: 84%

“…Attempts to swallow repeatedly fail, and the animals learn to stop responding (Susswein et al 1986;Schwarz et al 1988Schwarz et al , 1991Botzer et al 1998;Katzoff et al 2002Katzoff et al , 2006Katzoff et al , 2010Cohen-Armon et al 2004;Levitan et al 2010;Michel et al 2010Michel et al , 2011. Previous studies (Levitan et al 2008;Michel et al 2011Michel et al , 2012 used molecular markers of memory to localize the learning to specific ganglia. After training with inedible food, the markers were found in the buccal, but not in the cerebral, pleural, or pedal ganglia of Aplysia (Levitan et al 2008;Michel et al 2011).…”

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confidence: 99%

“…Previous studies (Levitan et al 2008;Michel et al 2011Michel et al , 2012 used molecular markers of memory to localize the learning to specific ganglia. After training with inedible food, the markers were found in the buccal, but not in the cerebral, pleural, or pedal ganglia of Aplysia (Levitan et al 2008;Michel et al 2011). The buccal ganglia contain a central pattern generator (CPG) organizing repetitive consummatory feeding behaviors, as well as motor neurons innervating buccal muscles (Elliott and Susswein 2002), which move the toothed radula (Ye et al 2006;Neustadter et al 2007).…”

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confidence: 99%

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Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

et al. 2012

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Training paradigms affecting Aplysia withdrawal reflexes cause changes in gene expression leading to long-term memory formation in primary mechanoafferents that initiate withdrawal. Similar mechanoafferents are also found in the buccal ganglia that control feeding behavior, raising the possibility that these mechanoafferents are a locus of memory formation after a training paradigm affecting feeding. Buccal ganglia mechanoafferent neurons expressed increases in mRNA expression for the transcription factor ApC/EBP, and for the growth factor sensorin-A, within the first 2 h after training with an inedible food. No increases in expression were detected in the rest of the buccal ganglia. Increased ApC/EBP expression was not elicited by food and feeding responses not causing long-term memory. Increased ApC/EBP expression was directly related to a measure of the efficacy of training in causing long-term memory, suggesting that ApC/EBP expression is necessary for the expression of aspects of long-term memory. In behaving animals, memory is expressed as a decrease in the likelihood to respond to food, and a decrease in the amplitude of protraction, the first phase of consummatory feeding behaviors.To determine how changes in the properties of mechanoafferents could cause learned changes in feeding behavior, synaptic contacts were mapped from the mechanoafferents to the B31/B32 neurons, which have a key role in initiating consummatory behaviors and also control protractions. Many mechanoafferents monosynaptically and polysynaptically connect with B31/B32. Monosynaptic connections were complex combinations of fast and slow excitation and/or inhibition. Changes in the response of B31/B32 to stimuli sensed by the mechanoafferent could underlie aspects of long-term memory expression.[Supplemental material is available for this article.]In a number of learning paradigms affecting Aplysia withdrawal reflexes, the connection from mechanoafferent neurons to effectors has been a major focus of research on how neural plasticity is translated into behavioral change (Byrne and

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“…More recently, hippocampal circadian rhythms in CREB activation have been shown to be dependent upon the Period1 gene (Rawashdeh et al 2014). In Aplysia, training animals during the subjective day results in significantly increased protein levels of the CREBdependent immediate early gene ApC/EBP (Lyons et al 2006), a transcription factor in nonassociative (Alberini et al 1994), and associative memory formation (Levitan et al 2008). In Drosophila mushroom bodies, a region necessary for many forms of memory, dCREB2 exhibits circadian oscillations in gene expression, nuclear protein levels and activity, likely mediating rhythms in LTM formation (Tanenhaus et al 2012;Fropf et al 2014).…”

Section: Micementioning

confidence: 99%

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

Krishnan

Lyons

2015

Learn. Mem.

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Circadian clocks evolved under conditions of environmental variation, primarily alternating light dark cycles, to enable organisms to anticipate daily environmental events and coordinate metabolic, physiological, and behavioral activities. However, modern lifestyle and advances in technology have increased the percentage of individuals working in phases misaligned with natural circadian activity rhythms. Endogenous circadian oscillators modulate alertness, the acquisition of learning, memory formation, and the recall of memory with examples of circadian modulation of memory observed across phyla from invertebrates to humans. Cognitive performance and memory are significantly diminished when occurring out of phase with natural circadian rhythms. Disruptions in circadian regulation can lead to impairment in the formation of memories and manifestation of other cognitive deficits. This review explores the types of interactions through which the circadian clock modulates cognition, highlights recent progress in identifying mechanistic interactions between the circadian system and the processes involved in memory formation, and outlines methods used to remediate circadian perturbations and reinforce circadian adaptation.Circadian clocks permit organisms to anticipate recurring daily environmental events through the coordination of metabolic, physiological, and behavioral rhythms. Conservation of the core principles through which circadian oscillators are organized across eukaryotic phyla suggests strong selective pressures for both circadian clocks and the mechanisms through which circadian oscillators operate. Intracellularly, transcription/translation feedback loops involving core circadian components set the stage for transcriptional regulation of thousands of genes in individual cells and tissues (Balsalobre et al.

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Training with inedible food in Aplysia causes expression of C/EBP in the buccal but not cerebral ganglion

Cited by 23 publications

References 51 publications

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

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

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