Olfactory habituation: Fresh insights from flies

Glanzman, David L.

doi:10.1073/pnas.1111230108

Cited by 19 publications

(15 citation statements)

References 17 publications

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“…There is evidence for such Hebbian potentiation of inhibitory synapses in other systems (Fischer and Carew, 1993;Bazhenov et al, 2005;Nugent et al, 2007;Fernandez et al, 2009;Rath et al, 2011). If this rule, which we propose for GABAergic synapses in the fly antennal lobe, were to be applied in other brain regions, then one would predict that persistent activity of a given ensemble of principal cells would result in synapse-specific strengthening of inhibitory inputs made onto these principal cells (Bazhenov et al, 2005;Das et al, 2011;Glanzman, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…We recently showed that cAMP-dependent plasticity of inhibitory transmission from the multiglomerular inhibitory local interneurons (LN1) subtype of interneurons in the antennal lobe mediates olfactory habituation (Das et al, 2011), a selective reduction in behavioral response to an odorant following sustained exposure (Glanzman, 2011). We ask here whether short-term olfactory habituation (STH) is: (1) driven by recurrent inhibition and (2) mediated by its plasticity.…”

Section: Introductionmentioning

confidence: 99%

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Plasticity of Recurrent Inhibition in theDrosophilaAntennal Lobe

Sudhakaran¹,

Holohan²,

Osman³

et al. 2012

J. Neurosci.

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Recurrent inhibition, wherein excitatory principal neurons stimulate inhibitory interneurons that feedback on the same principal cells, occurs ubiquitously in the brain. However, the regulation and function of recurrent inhibition are poorly understood in terms of the contributing interneuron subtypes as well as their effect on neural and cognitive outputs. In the Drosophila olfactory system, odorants activate olfactory sensory neurons (OSNs), which stimulate projection neurons (PNs) in the antennal lobe. Both OSNs and PNs activate local inhibitory neurons (LNs) that provide either feedforward or recurrent/feedback inhibition in the lobe. During olfactory habituation, prior exposure to an odorant selectively decreases the animal's subsequent response to the odorant. We show here that habituation occurs in response to feedback from PNs. Output from PNs is necessary for olfactory habituation and, in the absence of odorant, direct PN activation is sufficient to induce the odorant-selective behavioral attenuation characteristic of olfactory habituation. PN-induced habituation occludes further odor-induced habituation and similarly requires GABA A Rs and NMDARs in PNs, as well as VGLUT and cAMP signaling in the multiglomerular inhibitory local interneurons (LN1) type of LN. Thus, PN output is monitored by an LN subtype whose resultant plasticity underlies behavioral habituation. We propose that recurrent inhibitory motifs common in neural circuits may similarly underlie habituation to other complex stimuli.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Plasticity of Recurrent Inhibition in theDrosophilaAntennal Lobe

Sudhakaran¹,

Holohan²,

Osman³

et al. 2012

J. Neurosci.

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“…In Drosophila odor perception occurs on the level of olfactory neurons which express odor specific receptors and the broadly expressed general co-receptor Orco [5]; [6]. After activation of the olfactory neurons the signal is processed in the antennal lobes, a structure involved in transmission and habituation of olfactory information to the projection neurons [7]. The projection neurons in turn project to the lateral horn and the mushroom bodies, structures involved in associative olfactory learning and memory [8]; [9].…”

Section: Introductionmentioning

confidence: 99%

Neuronal Basis of Innate Olfactory Attraction to Ethanol in Drosophila

Schneider

Ruppert²,

Hendrich³

et al. 2012

PLoS ONE

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The decision to move towards a mating partner or a food source is essential for life. The mechanisms underlying these behaviors are not well understood. Here, we investigated the role of octopamine – the invertebrate analogue of noradrenaline – in innate olfactory attraction to ethanol. We confirmed that preference is caused via an olfactory stimulus by dissecting the function of the olfactory co-receptor Orco (formally known as OR83b). Orco function is not required for ethanol recognition per se, however it plays a role in context dependent recognition of ethanol. Odor-evoked ethanol preference requires the function of Tbh (Tyramine β hydroxalyse), the rate-limiting enzyme of octopamine synthesis. In addition, neuronal activity in a subset of octopaminergic neurons is necessary for olfactory ethanol preference. Notably, a specific neuronal activation pattern of tyraminergic/octopaminergic neurons elicit preference and is therefore sufficient to induce preference. In contrast, dopamine dependent increase in locomotor activity is not sufficient for olfactory ethanol preference. Consistent with the role of noradrenaline in mammalian drug induced rewards, we provide evidence that in adult Drosophila the octopaminergic neurotransmitter functions as a reinforcer and that the molecular dissection of the innate attraction to ethanol uncovers the basic properties of a response selection system.

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“…In insects, odorants are encoded by assemblies of projection neurons in the antennal lobe, a structure homologous to the mammalian olfactory bulb. Many lines of evidence argue that in a neutral environment, prolonged activation of an odorant-specific excitatory assembly results in the selective strengthening of inhibitory synapses onto neurons activated by the odorant (8,34). This strengthening of inhibitory synapses results in the formation of an inhibitory replica of the specific pattern of odor-induced excitation.…”

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 99%

Inhibitory engrams in perception and memory

Barron

Vogels

Behrens

et al. 2017

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

135

126

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Nervous systems use excitatory cell assemblies to encode and represent sensory percepts. Similarly, synaptically connected cell assemblies or "engrams" are thought to represent memories of past experience. Multiple lines of recent evidence indicate that brain systems create and use inhibitory replicas of excitatory representations for important cognitive functions. Such matched "inhibitory engrams" can form through homeostatic potentiation of inhibition onto postsynaptic cells that show increased levels of excitation. Inhibitory engrams can reduce behavioral responses to familiar stimuli, thereby resulting in behavioral habituation. In addition, by preventing inappropriate activation of excitatory memory engrams, inhibitory engrams can make memories quiescent, stored in a latent form that is available for contextrelevant activation. In neural networks with balanced excitatory and inhibitory engrams, the release of innate responses and recall of associative memories can occur through focused disinhibition. Understanding mechanisms that regulate the formation and expression of inhibitory engrams in vivo may help not only to explain key features of cognition but also to provide insight into transdiagnostic traits associated with psychiatric conditions such as autism, schizophrenia, and posttraumatic stress disorder.Percepts are thought to be represented in the brain by excitatory activity in groups of neurons, described as cell assemblies (1). Memories may similarly be represented by excitatory connections across different cell assemblies, which form when experiences trigger coordinated activity. Several recent studies indicate that the storage and reactivation of these excitatory "engrams" (2), respectively, may be accompanied by creation and modulation of matched inhibitory engrams. Here, we propose that inhibitory engrams, also termed "negative images" or "inhibitory representations," explain two fundamental features of animal and human psychology: first, behavioral habituation, which allows organisms to ignore familiar, frequently encountered percepts or stimuli, and, second, latent memory, wherein the brain stores tens of thousands of memories in a silent or latent state until recall is required. Such inhibitory engrams can be constructed in neural networks through simple, evolutionarily primitive, synaptic and cellular mechanisms, which are recognized to be involved in the phenomenon of excitatory-inhibitory (EI) balance observed across the brain.Neurons and neural circuits normally operate within a preset range of activity. Outside this range, altered levels of neuronal spiking trigger a variety of homeostatic mechanisms ranging from compensatory ion channel expression to local synaptic scaling (3, 4). These homeostatic mechanisms ensure that the activity parameters of a neuron operate around a set point such that the spiking rates remain stable and a balance of depolarizing and hyperpolarizing currents is maintained. As a consequence, excitation and inhibition are both locally and globally balanced, despite...

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Olfactory habituation: Fresh insights from flies

Cited by 19 publications

References 17 publications

Plasticity of Recurrent Inhibition in theDrosophilaAntennal Lobe

Plasticity of Recurrent Inhibition in theDrosophilaAntennal Lobe

Neuronal Basis of Innate Olfactory Attraction to Ethanol in Drosophila

Inhibitory engrams in perception and memory

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