Habituation as a neural algorithm for online odor discrimination

Shen, Yang; Dasgupta, Sanjoy; Navlakha, Saket

doi:10.1073/pnas.1915252117

Cited by 19 publications

(26 citation statements)

References 99 publications

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“…Two broad observations are relevant here. First, mechanisms underlying very short and longer lasting forms of habituation may differ, with the latter more likely to involve inhibitory potentiation (Ramaswami, 2014; Shen et al, 2020). Second, largely due to the difficulty of necessary behavioral experiments, in most instances where habituation override has been reported, it is not rigorously distinguished from a potential confounding process of response sensitization (Castellucci et al, 1970; Hawkins et al, 1998; Asztalos et al, 2007a; Asztalos et al, 2007b).…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Drosophila Circuit for Habituation Override

Trisal

Aranha

Chodankar

et al. 2021

Preprint

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Habituated animals retain a latent capacity for robust engagement with familiar stimuli. In most instances, the ability to override habituation is best explained by postulating: (a) that habituation arises from the potentiation of inhibitory inputs onto stimulus-encoding assemblies; and (b) fast habituation override occurs through disinhibition. Previous work has shown that inhibitory plasticity contributes to specific forms of olfactory and gustatory habituation in Drosophila. Here we analyze how exposure to a novel stimulus causes override of gustatory (proboscis-extension reflex or ″PER″) habituation. While brief sucrose contact with tarsal hairs causes naīve Drosophila to extend their proboscis, persistent tarsal exposure to sucrose reduces PER to subsequent sucrose stimuli. We show that in so habituated animals, either brief exposure of the proboscis to yeast or direct thermogenetic activation of sensory neurons restores the PER response to tarsal sucrose stimulation. Similar override of PER habituation can also be induced by brief thermogenetic activation of a population of TH (Tyrosine-Hydroxylase) positive neurons, a subset of which send projections to the SEZ. Significantly, sensory-neuron induced habituation override requires transmitter release from these TH-positive cells. Treatments that cause override specifically influence the habituated state, with no effect on the naīve sucrose response across a range of concentrations. Taken together, these and other findings are consistent with a model in which novel taste stimuli trigger activity in dopaminergic neurons which, directly or indirectly, inhibit GABAergic cells that drive PER habituation. The implications of these findings for general mechanisms of attentional and sensory override of habituation are discussed.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Drosophila Circuit for Habituation Override

Trisal

Aranha

Chodankar

et al. 2021

Preprint

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“…A neuronal algorithm implicating inhibitory potentiation of habituation should also be able to make predictions and efficiently detect salient features in the environment [54]. The "negativeimage model" as defined by Ramaswami can thus serve as a general mechanism for adaptive filtering, generation of predictions and saliency mapping.…”

Section: Habituation Mechanismsmentioning

confidence: 99%

Genetics, Molecular Control and Clinical Relevance of Habituation Learning

Blok¹,

Boon²,

Reijmersdal³

et al. 2022

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Habituation, the most ancient and fundamental form of learning, manifests already before birth. Neuroscientists have been fascinated for decades by its function as a firewall protecting our brains from sensory information overload and its indispensability for higher cognitive processing. Evidence that habituation learning is affected in autism and related monogenic neurodevelopmental syndromes and their animal models has exponentially grown, but the potential of this convergence to advance both fields is still largely unexploited.In this review, we provide a systematic overview of the genes that to date have been demonstrated to underlie habituation across species. We describe the biological processes they converge on, and highlight core regulatory pathways and repurposable drugs that may alleviate the habituation deficits associated with their dysregulation. We also summarize currently used habituation paradigms and extract the most important arguments from literature that support the crucial role of habituation for cognition in health and disease. We conclude that habituation is a powerful tool to overcome current bottlenecks in research, diagnostics and treatment of neurodevelopmental disorders.

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“…Two broad observations are relevant here. First, mechanisms underlying very short and longer lasting forms of habituation may differ; some forms of the latter are known to involve inhibitory potentiation (Ramaswami, 2014;Shen et al, 2020). Second, largely because of the difficulty of necessary behavioral experiments, in most (but not all, Semelidou et al, 2018) instances, habituation override is not distinguished from a potential confounding process of response sensitization (Castellucci et al, 1970;Hawkins et al, 1998;Asztalos et al, 2007a,b).…”

Section: Introductionmentioning

confidence: 99%

ADrosophilaCircuit for Habituation Override

et al. 2022

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Habituated animals retain a latent capacity for robust engagement with familiar stimuli. In most instances, the ability to override habituation is best explained by postulating that habituation arises from the potentiation of inhibitory inputs onto stimulus-encoding assemblies and that habituation override occurs through disinhibition. Previous work has shown that inhibitory plasticity contributes to specific forms of olfactory and gustatory habituation in Drosophila. Here, we analyze how exposure to a novel stimulus causes override of gustatory (proboscis extension reflex; PER) habituation. While brief sucrose contact with tarsal hairs causes naive Drosophila to extend their proboscis, persistent exposure reduces PER to subsequent sucrose stimuli. We show that in so habituated animals, either brief exposure of the proboscis to yeast or direct thermogenetic activation of sensory neurons restores PER response to tarsal sucrose stimulation. Similar override of PER habituation can also be induced by brief thermogenetic activation of a population of tyrosine hydroxylase (TH)-positive neurons, a subset of which send projections to the subesophageal zone (SEZ). Significantly, sensory-neuron induced habituation override requires transmitter release from these TH-positive cells. Treatments that cause override specifically influence the habituated state, with no effect on the naive sucrose response across a range of concentrations. Taken together with other findings, these observations in female flies are consistent with a model in which novel taste stimuli trigger activity in dopaminergic neurons which, directly or indirectly, inhibit GABAergic cells that drive PER habituation. The implications of these findings for general mechanisms of attentional and sensory override of habituation are discussed.

show abstract

Habituation as a neural algorithm for online odor discrimination

Cited by 19 publications

References 99 publications

A Drosophila Circuit for Habituation Override

A Drosophila Circuit for Habituation Override

Genetics, Molecular Control and Clinical Relevance of Habituation Learning

ADrosophilaCircuit for Habituation Override

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