Long-Term Memory Leads to Synaptic Reorganization in the Mushroom Bodies: A Memory Trace in the Insect Brain?

A novel encoding hypothesis that explains proactive inhibition in the Brown-Peterson paradigm was developed and tested in three experiments. This hypothesis argues that initial recall on each trial activates a pool of associates and the encoding of the next trial occurs during such activation. The encoding is facilitated and leaves a weak long-term memory trace. Build-up and release of inhibition, as well as a number of other typical results, are parsimoniously accounted for by such a mechanism. In support of the hypothesis, Exps. 1 and 2 demonstrated significant accentuation of proactive inhibition with increased activation both in the presence and absence of inter-trial category relationship. Exp. 3 showed significant attenuation of proactive inhibition as activation decayed. Increase in latency of recall with increased activation was also noted.

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Impairments to Consolidation, Reconsolidation, and Long-Term Memory Maintenance Lead to Memory Erasure

Annual Review of Neuroscience ◽

10.1146/annurev-neuro-091319-024636 ◽

2020 ◽

Vol 43 (1) ◽

pp. 297-314 ◽

Cited By ~ 2

Author(s):

Josué Haubrich ◽

Matteo Bernabo ◽

Andrew G. Baker ◽

Karim Nader

Keyword(s):

Memory Trace ◽

Direct Approach ◽

Long Term Memory ◽

Retrieval Failure ◽

Term Memory ◽

The Brain

An enduring problem in neuroscience is determining whether cases of amnesia result from eradication of the memory trace (storage impairment) or if the trace is present but inaccessible (retrieval impairment). The most direct approach to resolving this question is to quantify changes in the brain mechanisms of long-term memory (BM-LTM). This approach argues that if the amnesia is due to a retrieval failure, BM-LTM should remain at levels comparable to trained, unimpaired animals. Conversely, if memories are erased, BM-LTM should be reduced to resemble untrained levels. Here we review the use of BM-LTM in a number of studies that induced amnesia by targeting memory maintenance or reconsolidation. The literature strongly suggests that such amnesia is due to storage rather than retrieval impairments. We also describe the shortcomings of the purely behavioral protocol that purports to show recovery from amnesia as a method of understanding the nature of amnesia.

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The Biochemical Basis of Long-Term Memory

Quarterly Reviews of Biophysics ◽

10.1017/s0033583500000937 ◽

1969 ◽

Vol 2 (2) ◽

pp. 135-173 ◽

Cited By ~ 30

Author(s):

Richard B. Roberts ◽

Louis B. Flexner

Keyword(s):

Learning And Memory ◽

Memory Trace ◽

Practical Interest ◽

Long Term Memory ◽

Daily Lives ◽

Biochemical Basis ◽

Term Memory ◽

Actual Knowledge

Learning and memory are important elements of our daily lives, familiar to all through introspection. Yet the mechanisms underlying these processes are still for the most part unknown. Here are problems which combine a maximum of intrinsic and practical interest with a minimum of actual knowledge and understanding. Years of our lives are dedicated to the formation of certain long-term memories and behaviour patterns, yet we have only rudimentary notions of how such ‘schooling’ is best accomplished. There is no certainty in any aspect of the process. We are not sure whether relatively few cells or millions participate in a memory trace; whether these cells change as a whole, or whether the changes are limited to synaptic regions. In fact, we cannot be certain whether the changes are confined to the neurones or whether the glia also participate.

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Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies

Nature Communications ◽

10.1038/ncomms13471 ◽

2016 ◽

Vol 7 (1) ◽

Cited By ~ 35

Author(s):

Yukinori Hirano ◽

Kunio Ihara ◽

Tomoko Masuda ◽

Takuya Yamamoto ◽

Ikuko Iwata ◽

...

Keyword(s):

Mushroom Bodies ◽

Long Term Memory ◽

Term Memory ◽

Transcriptional Machinery

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Appetitive learning relies on octopamine and dopamine in ants

10.1101/2021.04.19.438615 ◽

2021 ◽

Author(s):

Maarten Wissink ◽

Volker Nehring

Keyword(s):

Short Term Memory ◽

Receptor Blocker ◽

Lasius Niger ◽

Insect Brain ◽

Long Term Memory ◽

Term Memory ◽

Appetitive Learning ◽

Octopamine Receptors ◽

Octopamine Receptor

Associative learning relies on the detection of coincidence between a stimulus and a reward or punishment. In the insect brain, this process is thought to be carried out in the mushroom bodies under control of octopaminergic and dopaminergic neurons. It was assumed that appetitive learning is governed by octopaminergic neurons, while dopamine is required for aversive learning. This view has been recently challenged: Both neurotransmitters seem to be involved in both types of memory in bees and flies. Here, we test which neurotransmitters are required for appetitive learning in ants. We trained Lasius niger ant workers to discriminate two mixtures of linear hydrocarbons and associate one of them with a sucrose reward. We analysed the behaviour of the trained ants using machine learning and found that they preferred the rewarded odour over the other, a preference that was stable for at least 24 hours. We then treated the ants before learning with either epinastine, an octopamine receptor blocker, or with flupentixol, a dopamine receptor blocker. Ants with blocked octopamine receptors did not remember the rewarded odour. Octopamine signalling is thus necessary for the formation of appetitive memory. In contrast, ants with blocked dopamine receptors initially learned the rewarded odour but failed to retrieve this memory 24 hours later. Dopamine is thus required for long-term memory consolidation during appetitive conditioning, independent of short-term memory formation. Our results show that appetitive learning depends on both octopamine and dopamine signalling in ants.

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The pharmacology of long-term memory

European Review ◽

10.1017/s1062798700001319 ◽

1995 ◽

Vol 3 (1) ◽

pp. 35-48 ◽

Cited By ~ 2

Author(s):

Cesare Mondadori

Keyword(s):

Memory Trace ◽

Long Term Memory ◽

Drug Induced ◽

Term Memory ◽

Memory Enhancing ◽

Better Than

If information enters memory under the influence of a memory-enhancing substance, for about 16 hours thereafter the recollection of that information is no better than if it had been acquired without any treatment. Later tests of retention, however, performed one or more days, or even weeks, after the experience, show a drug-induced improvement of memory. Memory-enhancing compounds thus appear to facilitate the formation of the long-term memory trace. On the assumption that differences between treated and untreated animals emerge from that moment on when memory is based on the products of the processes modulated by the drugs, it can be postulated that long-term memory comes into play after about 16–20 hours.

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A kinase-dependent feedforward loop affects CREBB stability and long term memory formation

eLife ◽

10.7554/elife.33007 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 6

Author(s):

Pei-Tseng Lee ◽

Guang Lin ◽

Wen-Wen Lin ◽

Fengqiu Diao ◽

Benjamin H White ◽

...

Keyword(s):

Aversive Conditioning ◽

Memory Deficits ◽

Memory Formation ◽

Mushroom Bodies ◽

Limiting Factor ◽

Long Term Memory ◽

Term Memory ◽

Feedforward Loop ◽

Genes Encoding

In Drosophila, long-term memory (LTM) requires the cAMP-dependent transcription factor CREBB, expressed in the mushroom bodies (MB) and phosphorylated by PKA. To identify other kinases required for memory formation, we integrated Trojan exons encoding T2A-GAL4 into genes encoding putative kinases and selected for genes expressed in MB. These lines were screened for learning/memory deficits using UAS-RNAi knockdown based on an olfactory aversive conditioning assay. We identified a novel, conserved kinase, Meng-Po (MP, CG11221, SBK1 in human), the loss of which severely affects 3 hr memory and 24 hr LTM, but not learning. Remarkably, memory is lost upon removal of the MP protein in adult MB but restored upon its reintroduction. Overexpression of MP in MB significantly increases LTM in wild-type flies showing that MP is a limiting factor for LTM. We show that PKA phosphorylates MP and that both proteins synergize in a feedforward loop to control CREBB levels and LTM. key words: Drosophila, Mushroom bodies, SBK1, deGradFP, T2A-GAL4, MiMIC

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Consolidation and maintenance of long-term memory involve dual functions of the developmental regulator Apterous in clock neurons and mushroom bodies in the Drosophila brain

PLoS Biology ◽

10.1371/journal.pbio.3001459 ◽

2021 ◽

Vol 19 (12) ◽

pp. e3001459

Author(s):

Show Inami ◽

Tomohito Sato ◽

Yuto Kurata ◽

Yuki Suzuki ◽

Toshihiro Kitamoto ◽

...

Keyword(s):

Memory Consolidation ◽

Ex Vivo ◽

Adult Brain ◽

Mushroom Bodies ◽

Long Term Memory ◽

Gamma Aminobutyric Acid ◽

Behavioral Arousal ◽

Term Memory ◽

Dual Functions

Memory is initially labile but can be consolidated into stable long-term memory (LTM) that is stored in the brain for extended periods. Despite recent progress, the molecular and cellular mechanisms underlying the intriguing neurobiological processes of LTM remain incompletely understood. Using the Drosophila courtship conditioning assay as a memory paradigm, here, we show that the LIM homeodomain (LIM-HD) transcription factor Apterous (Ap), which is known to regulate various developmental events, is required for both the consolidation and maintenance of LTM. Interestingly, Ap is involved in these 2 memory processes through distinct mechanisms in different neuronal subsets in the adult brain. Ap and its cofactor Chip (Chi) are indispensable for LTM maintenance in the Drosophila memory center, the mushroom bodies (MBs). On the other hand, Ap plays a crucial role in memory consolidation in a Chi-independent manner in pigment dispersing factor (Pdf)-containing large ventral–lateral clock neurons (l-LNvs) that modulate behavioral arousal and sleep. Since disrupted neurotransmission and electrical silencing in clock neurons impair memory consolidation, Ap is suggested to contribute to the stabilization of memory by ensuring the excitability of l-LNvs. Indeed, ex vivo imaging revealed that a reduced function of Ap, but not Chi, results in exaggerated Cl− responses to the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) in l-LNvs, indicating that wild-type (WT) Ap maintains high l-LNv excitability by suppressing the GABA response. Consistently, enhancing the excitability of l-LNvs by knocking down GABAA receptors compensates for the impaired memory consolidation in ap null mutants. Overall, our results revealed unique dual functions of the developmental regulator Ap for LTM consolidation in clock neurons and LTM maintenance in MBs.

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