Acute Disruption of the NMDA Receptor Subunit NR1 in the Honeybee Brain Selectively Impairs Memory Formation

Müssig, Laurenz; Richlitzki, Antje; Rössler, Reinhard; Eisenhardt, Dorothea; Menzel, Randolf; Leboulle, Gérard

doi:10.1523/jneurosci.5543-09.2010

Cited by 62 publications

(38 citation statements)

References 44 publications

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“…Although the neuro-excitatory functions of glutamate interacting with N-methyl-D-aspartic acid (NMDA) receptors found at the post-synaptic membrane have been well studied in both vertebrates and invertebrates, the function of D-and L-aspartic acid and their conversions to NMDA 37,40 is less well understood. Importantly, glutamatergic neurons are found in the mushroom bodies of the honeybee brain, and glutamate and NMDA receptors have been shown to play a role in LTM formation in honeybees [41][42][43] . Thus, our finding that asparagine synthetase is downregulated after olfactory conditioning in bees provides an important addition to current knowledge on the molecular processes regulating learning and memory in this insect model 15,27,44 .…”

Section: Discussionmentioning

confidence: 99%

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

et al. 2014

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Increasing evidence suggests small non-coding RNAs (ncRNAs) such as microRNAs (miRNAs) control levels of mRNA expression during experience-related remodelling of the brain. Here we use an associative olfactory learning paradigm in the honeybee Apis mellifera to examine gene expression changes in the brain during memory formation. Brain transcriptome analysis reveals a general downregulation of protein-coding genes, including asparagine synthetase and actin, and upregulation of ncRNAs. miRNA-mRNA network predictions together with PCR validation suggest miRNAs including miR-210 and miR-932 target the downregulated protein-coding genes. Feeding cholesterol-conjugated antisense RNA to bees results in the inhibition of miR-210 and of miR-932. Loss of miR-932 impairs long-term memory formation, but not memory acquisition. Functional analyses show that miR-932 interacts with Act5C, providing evidence for direct regulation of actin expression by an miRNA. An activity-dependent increase in miR-932 expression may therefore control actin-related plasticity mechanisms and affect memory formation in the brain.

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Section: Discussionmentioning

confidence: 99%

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

et al. 2014

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“…A recent study has shown, for instance, that the NMDA receptor, which acts as a sensor of coincident activity between neural inputs and whose activation during learning is considered important for various forms of memory, also contributes to memory differentiation in bees (Mussig et al 2010). When the expression of the NR1 subunit of the NMDA receptor was inhibited in the mushroom bodies using RNA interference, an impairment of both MTM and e-LTM was found, while l-LTM was left intact (for further analyses coupling PER conditioning and molecular interferences, see Schwärzel and Müller 2006).…”

Section: Neural Bases Of Cs and Us Processingmentioning

confidence: 99%

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Giurfa

Sandoz²

2012

Learn. Mem.

338

334

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The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.Classical conditioning (Pavlov 1927) is a form of conditioning in which a subject learns to associate a neutral stimulus (the "conditioned stimulus," or CS), which does not originally elicit a behavioral response, with a stimulus of biological significance (the "unconditioned stimulus," or US), which elicits an innate, often reflexive, response. Through this association, the originally neutral stimulus acquires the capacity to elicit a conditioned response.Decades of research on animal learning and memory have established some invertebrates (e.g., the sea hare, Aplysia californica, the fruit fly, Drosophila melanogaster, the honeybee, Apis mellifera) as standard models for the study of classical conditioning (Giurfa 2007b;Menzel et al. 2007). This success can be attributed to the fact that these animals can learn nonassociative as well as Pavlovian and operant associations and possess relatively simple nervous systems that allow retracing of these phenomena to the cellular and molecular levels in different kinds of laboratory preparations. Among these invertebrates, the honeybee, Apis mellifera, has emerged as a robust and influential model for the study of

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“…It has also been linked to investigations of the genetic basis of differences in learning 28,29 , the physiological correlates of olfactory perception and memory in the brain 13,14,30 , and the modulatory and molecular genetic bases of behavior 15,16,31 . Because of the advanced knowledge of the ecological relevance of olfactory learning to honey bees, which started with the first studies by Karl von Frisch The basic procedure is powerful in that it can be applied to investigate problems in other species as well.…”

Section: Discussionmentioning

confidence: 99%

A Proboscis Extension Response Protocol for Investigating Behavioral Plasticity in Insects: Application to Basic, Biomedical, and Agricultural Research

Smith

Burden

2014

JoVE

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Insects modify their responses to stimuli through experience of associating those stimuli with events important for survival (e.g., food, mates, threats). There are several behavioral mechanisms through which an insect learns salient associations and relates them to these events. It is important to understand this behavioral plasticity for programs aimed toward assisting insects that are beneficial for agriculture. This understanding can also be used for discovering solutions to biomedical and agricultural problems created by insects that act as disease vectors and pests. The Proboscis Extension Response (PER) conditioning protocol was developed for honey bees (Apis mellifera) over 50 years ago to study how they perceive and learn about floral odors, which signal the nectar and pollen resources a colony needs for survival. The PER procedure provides a robust and easy-to-employ framework for studying several different ecologically relevant mechanisms of behavioral plasticity. It is easily adaptable for use with several other insect species and other behavioral reflexes. These protocols can be readily employed in conjunction with various means for monitoring neural activity in the CNS via electrophysiology or bioimaging, or for manipulating targeted neuromodulatory pathways. It is a robust assay for rapidly detecting sub-lethal effects on behavior caused by environmental stressors, toxins or pesticides.We show how the PER protocol is straightforward to implement using two procedures. One is suitable as a laboratory exercise for students or for quick assays of the effect of an experimental treatment. The other provides more thorough control of variables, which is important for studies of behavioral conditioning. We show how several measures for the behavioral response ranging from binary yes/no to more continuous variable like latency and duration of proboscis extension can be used to test hypotheses. And, we discuss some pitfalls that researchers commonly encounter when they use the procedure for the first time.

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Acute Disruption of the NMDA Receptor Subunit NR1 in the Honeybee Brain Selectively Impairs Memory Formation

Cited by 62 publications

References 44 publications

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

A Proboscis Extension Response Protocol for Investigating Behavioral Plasticity in Insects: Application to Basic, Biomedical, and Agricultural Research

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