Neurobiology of a Simple Memory

Wilson, Donald A.; Linster, Christiane

doi:10.1152/jn.90479.2008

Cited by 100 publications

(99 citation statements)

References 63 publications

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“…Several studies have documented both non-associative and associative plasticity in early olfactory processing in mammalian and insect brains (Fernandez et al, 2009;Locatelli et al, 2013;Wilson and Linster, 2008). However, studies have not addressed why this plasticity exists in relation to the ecological problem it helps to solve.…”

Section: Discussionmentioning

confidence: 99%

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

Locatelli

Fernández

Smith

2016

Journal of Experimental Biology

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Natural odors are typically mixtures of several chemical components.Mixtures vary in composition among odor objects that have the same meaning. Therefore a central 'categorization' problem for an animal as it makes decisions about odors in natural contexts is to correctly identify odor variants that have the same meaning and avoid variants that have a different meaning. We propose that identified mechanisms of associative and non-associative plasticity in early sensory processing in the insect antennal lobe and mammalian olfactory bulb are central to solving this problem. Accordingly, this plasticity should work to improve categorization of odors that have the opposite meanings in relation to important events. Using synthetic mixtures designed to mimic natural odor variation among flowers, we studied how honey bees learn about and generalize among floral odors associated with food. We behaviorally conditioned honey bees on a difficult odor discrimination problem using synthetic mixtures that mimic natural variation among snapdragon flowers. We then used calcium imaging to measure responses of projection neurons of the antennal lobe, which is the first synaptic relay of olfactory sensory information in the brain, to study how ensembles of projection neurons change as a result of behavioral conditioning. We show how these ensembles become 'tuned' through plasticity to improve categorization of odors that have the different meanings. We argue that this tuning allows more efficient use of the immense coding space of the antennal lobe and olfactory bulb to solve the categorization problem. Our data point to the need for a better understanding of the 'statistics' of the odor space.

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Section: Discussionmentioning

confidence: 99%

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

Locatelli

Fernández

Smith

2016

Journal of Experimental Biology

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“…It provides a filtering mechanism, which is an important prerequisite for higher cognitive functioning. 31,32 Using the light-off jump reflex habituation, we have previously identified learning deficits in number of Drosophila ID models. 9,24,26 Two independent inducible RNAi lines targeting the Drosophila WAC orthologue CG8949 (vdrc48307 and vdrc107328) and their corresponding genetic background control lines (vdrc60000 and vdrc60100) were obtained (Vienna Drosophila RNAi Center 22 ) and fly stocks were kept under standard conditions.…”

Section: Panneuronal Knockdown Of the Drosophila Wac Orthologue Resulmentioning

confidence: 99%

De novo loss-of-function mutations in WAC cause a recognizable intellectual disability syndrome and learning deficits in Drosophila

et al. 2016

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Recently WAC was reported as a candidate gene for intellectual disability (ID) based on the identification of a de novo mutation in an individual with severe ID. WAC regulates transcription-coupled histone H2B ubiquitination and has previously been implicated in the 10p12p11 contiguous gene deletion syndrome. In this study, we report on 10 individuals with de novo WAC mutations which we identified through routine (diagnostic) exome sequencing and targeted resequencing of WAC in 2326 individuals with unexplained ID. All but one mutation was expected to lead to a loss-of-function of WAC. Clinical evaluation of all individuals revealed phenotypic overlap for mild ID, hypotonia, behavioral problems and distinctive facial dysmorphisms, including a square-shaped face, deep set eyes, long palpebral fissures, and a broad mouth and chin. These clinical features were also previously reported in individuals with 10p12p11 microdeletion syndrome. To investigate the role of WAC in ID, we studied the importance of the Drosophila WAC orthologue (CG8949) in habituation, a non-associative learning paradigm. Neuronal knockdown of Drosophila CG8949 resulted in impaired learning, suggesting that WAC is required in neurons for normal cognitive performance. In conclusion, we defined a clinically recognizable ID syndrome, caused by de novo loss-of-function mutations in WAC. Independent functional evidence in Drosophila further supported the role of WAC in ID. On the basis of our data WAC can be added to the list of ID genes with a role in transcription regulation through histone modification.

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“…Furthermore, less is known about the consequences of peripheral adaptation in perceptual habituation or desensitization, an everyday experience in olfaction (for review, see Wilson and Linster, 2008). In the first and second relays of olfaction, i.e., in the olfactory bulb and the pyriform cortex, neurons do adapt (Wilson, 1998;Sobel et al, 2000;Schafer et al, 2005); however, the precise role of ORN adaptation versus local network processing in the decrement of central neuron responses is unclear.…”

Section: Introductionmentioning

confidence: 99%

Peripheral Adaptation Codes for High Odor Concentration in Glomeruli

Lecoq¹,

Tiret²,

Charpak³

2009

J. Neurosci.

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Adaptation is a general property of sensory receptor neurons and has been extensively studied in isolated cell preparation of olfactory receptor neurons. In contrast, little is known about the conditions under which peripheral adaptation occurs in the CNS during odorant stimulation. Here, we used two-photon laser-scanning microscopy and targeted extracellular recording in freely breathing anesthetized rats to investigate the correlate of peripheral adaptation at the first synapse of the olfactory pathway in olfactory bulb glomeruli. We find that during sustained stimulation at high concentration, odorants can evoke local field potential (LFP) postsynaptic responses that rapidly adapt with time, some within two inhalations. Simultaneous measurements of LFP and calcium influx at olfactory receptor neuron terminals reveal that postsynaptic adaptation is associated with a decrease in odorant-evoked calcium response, suggesting that it results from a decrease in glutamate release. This glomerular adaptation was concentration-dependent and did not change the glomerular input-output curve. In addition, in situ application of antagonists of either ionotropic glutamate receptors or metabotropic GABA B receptors did not affect this adaptation, thus discarding the involvement of local presynaptic inhibition. Glomerular adaptation, therefore, reflects the response decline of olfactory receptor neurons to sustained odorant. We postulate that peripheral fast adaptation is a means by which glomerular output codes for high concentration of odor.

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Neurobiology of a Simple Memory

Cited by 100 publications

References 63 publications

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

De novo loss-of-function mutations in WAC cause a recognizable intellectual disability syndrome and learning deficits in Drosophila

Peripheral Adaptation Codes for High Odor Concentration in Glomeruli

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