Internal state configures olfactory behavior and early sensory processing in Drosophila larvae

Animals exhibit different behavioral responses to the same sensory cue depending on their internal state at a given moment. How and where in the brain are sensory inputs combined with state information to select an appropriate behavior? Here, we investigate how food deprivation affects olfactory behavior in Drosophila larvae. We find that certain odors repel well-fed animals but attract food-deprived animals and that feeding state flexibly alters neural processing in the first olfactory center, the antennal lobe. Hunger differentially modulates two output pathways required for opposing behavioral responses. Upon food deprivation, attraction-mediating uniglomerular projection neurons show elevated odor-evoked activity, whereas an aversion-mediating multiglomerular projection neuron receives odor-evoked inhibition. The switch between these two pathways is regulated by the lone serotonergic neuron in the antennal lobe, CSD. Our findings demonstrate how flexible behaviors can arise from state-dependent circuit dynamics in an early sensory processing center.

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Internal state configures olfactory behavior and early sensory processing in Drosophila larvae

10.1101/2020.03.02.973941 ◽

2020 ◽

Cited By ~ 3

Author(s):

Katrin Vogt ◽

David M. Zimmerman ◽

Matthias Schlichting ◽

Luis Hernandez-Nunez ◽

Shanshan Qin ◽

...

Keyword(s):

Food Deprivation ◽

Sensory Processing ◽

Antennal Lobe ◽

Internal State ◽

Behavioral Responses ◽

Projection Neuron ◽

Projection Neurons ◽

Olfactory Behavior ◽

Odor Aversion ◽

Odor Attraction

Animals exhibit different behavioral responses to the same sensory cue depending on their state at a given moment in time. How and where in the brain are sensory inputs combined with internal state information to select an appropriate behavior? Here we investigate how food deprivation affects olfactory behavior in Drosophila larvae. We find that certain odors reliably repel well-fed animals but attract food-deprived animals. We show that feeding state flexibly alters neural processing in the first olfactory center, the antennal lobe. Food deprivation differentially modulates two separate output pathways that are required for opposing behavioral responses. Uniglomerular projection neurons mediate odor attraction and show elevated odor-evoked activity in the food-deprived state. A multiglomerular projection neuron mediates odor aversion and receives odor-evoked inhibition in the food-deprived state. The switch between these two pathways is regulated by the lone serotonergic neuron in the antennal lobe, CSD. Our findings demonstrate how flexible behaviors can arise from state-dependent circuit dynamics in an early sensory processing center.

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Experience-dependent plasticity modulates ongoing activity in the antennal lobe and enhance odor representations

10.1101/2021.04.28.441745 ◽

2021 ◽

Author(s):

Luis M. Franco ◽

Emre Yaksi

Keyword(s):

Antennal Lobe ◽

Internal State ◽

Brain Activity ◽

Fruit Fly ◽

Brain Regions ◽

Projection Neurons ◽

Ongoing Activity ◽

Dependent Plasticity ◽

Olfactory Glomeruli ◽

The Brain

ABSTRACTOngoing neural activity has been observed across several brain regions and thought to reflect the internal state of the brain. Yet, it is not fully understood how ongoing brain activity interacts with sensory experience and shape sensory representations. Here, we show that projection neurons of the fruit fly antennal lobe exhibit spatiotemporally organized ongoing activity in the absence of odor stimulation. Upon repeated exposure to odors, we observe a gradual and long-lasting decrease in the amplitude and frequency of spontaneous calcium events, as well as a reorganization of correlations between olfactory glomeruli during ongoing activity. Accompanying these plastic changes, we find that repeated odor experience reduces trial-to-trial variability and enhances the specificity of odor representations. Our results reveal a previously undescribed experience-dependent plasticity of ongoing and sensory driven activity at peripheral levels of the fruit fly olfactory system.

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Functional and Anatomical Specificity in a Higher Olfactory Centre

10.1101/336982 ◽

2018 ◽

Cited By ~ 5

Author(s):

Shahar Frechter ◽

Alexander S. Bates ◽

Sina Tootoonian ◽

Michael-John Dolan ◽

James D. Manton ◽

...

Keyword(s):

Sensory Processing ◽

Mushroom Body ◽

Cell Types ◽

Projection Neurons ◽

Olfactory Behavior ◽

Population Code ◽

Odor Coding ◽

Sensory Stimuli ◽

Anatomical Analysis ◽

Sparse Population

AbstractMost sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. For example, in insects, second order olfactory projection neurons target both the mushroom body, which is required for learning, and the lateral horn (LH), which has been proposed to mediate innate olfactory behavior. Mushroom body neurons encode odors in a sparse population code, which does not appear stereotyped across animals. In contrast the functional principles of odor coding in the LH remain poorly understood. We have carried out a comprehensive anatomical analysis of the Drosophila LH, counting ~1400 neurons; combining genetic driver lines, anatomical and functional criteria, we identify 165 LHN cell types. We then show that genetically labeled LHNs have stereotyped odor responses across animals for 33 of these cell types. LHN tuning can be ultra-sparse (1/40 odors tested), but on average single LHNs respond to three times more odors than single projection neurons. This difference can be rationalized by our observation that LHNs are better odor categorizers, likely due to pooling of input projection neurons responding to different odors of the same category. Our results reveal some of the principles by which a higher sensory processing area can extract innate behavioral significance from sensory stimuli.

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Faculty Opinions recommendation of Internal state configures olfactory behavior and early sensory processing in Drosophila larvae.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.739289002.793586544 ◽

2021 ◽

Author(s):

Martin Giurfa

Keyword(s):

Sensory Processing ◽

Internal State ◽

Olfactory Behavior ◽

Drosophila Larvae

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Sparsening and Temporal Sharpening of Olfactory Representations in the Honeybee Mushroom Bodies

Journal of Neurophysiology ◽

10.1152/jn.00397.2005 ◽

2005 ◽

Vol 94 (5) ◽

pp. 3303-3313 ◽

Cited By ~ 107

Author(s):

Paul Szyszka ◽

Mathias Ditzen ◽

Alexander Galkin ◽

C. Giovanni Galizia ◽

Randolf Menzel

Keyword(s):

Mushroom Body ◽

Antennal Lobe ◽

Activity Patterns ◽

Projection Neuron ◽

Insect Brain ◽

Projection Neurons ◽

Similar Response ◽

Kenyon Cell ◽

Cell Responses ◽

Kenyon Cells

We explored the transformations accompanying the transmission of odor information from the first-order processing area, the antennal lobe, to the mushroom body, a higher-order integration center in the insect brain. Using Ca2+ imaging, we recorded activity in the dendrites of the projection neurons that connect the antennal lobe with the mushroom body. Next, we recorded the presynaptic terminals of these projection neurons. Finally, we characterized their postsynaptic partners, the intrinsic neurons of the mushroom body, the clawed Kenyon cells. We found fundamental differences in odor coding between the antennal lobe and the mushroom body. Odors evoked combinatorial activity patterns at all three processing stages, but the spatial patterns became progressively sparser along this path. Projection neuron dendrites and boutons showed similar response profiles, but the boutons were more narrowly tuned to odors. The transmission from projection neuron boutons to Kenyon cells was accompanied by a further sparsening of the population code. Activated Kenyon cells were highly odor specific. Furthermore, the onset of Kenyon cell responses to projection neurons occurred within the first 200 ms and complex temporal patterns were transformed into brief phasic responses. Thus two types of transformations occurred within the MB: sparsening of a combinatorial code, mediated by pre- and postsynaptic processing within the mushroom body microcircuits, and temporal sharpening of postsynaptic Kenyon cell responses, probably involving a broader loop of inhibitory recurrent neurons.

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Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits

eLife ◽

10.7554/elife.08298 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 71

Author(s):

Kang I Ko ◽

Cory M Root ◽

Scott A Lindsay ◽

Orel A Zaninovich ◽

Andrew K Shepherd ◽

...

Keyword(s):

Antennal Lobe ◽

Neural Circuits ◽

Internal State ◽

Animal Cognition ◽

Olfactory Behavior ◽

Enhanced Sensitivity ◽

Functional Remodeling ◽

Olfactory Processing ◽

Toxic Food ◽

And Behavior

The internal state of an organism influences its perception of attractive or aversive stimuli and thus promotes adaptive behaviors that increase its likelihood of survival. The mechanisms underlying these perceptual shifts are critical to our understanding of how neural circuits support animal cognition and behavior. Starved flies exhibit enhanced sensitivity to attractive odors and reduced sensitivity to aversive odors. Here, we show that a functional remodeling of the olfactory map is mediated by two parallel neuromodulatory systems that act in opposing directions on olfactory attraction and aversion at the level of the first synapse. Short neuropeptide F sensitizes an antennal lobe glomerulus wired for attraction, while tachykinin (DTK) suppresses activity of a glomerulus wired for aversion. Thus we show parallel neuromodulatory systems functionally reconfigure early olfactory processing to optimize detection of nutrients at the risk of ignoring potentially toxic food resources.

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Communication from learned to innate olfactory processing centers is required for memory retrieval in Drosophila

10.1101/167312 ◽

2017 ◽

Cited By ~ 4

Author(s):

Michael-John Dolan ◽

Ghislain Belliart-Guérin ◽

Alexander Shakeel Bates ◽

Yoshinori Aso ◽

Shahar Frechter ◽

...

Keyword(s):

Behavioral Response ◽

Memory Retrieval ◽

Mushroom Body ◽

Behavioral Responses ◽

Cell Types ◽

Olfactory Behavior ◽

Olfactory Neurons ◽

Appropriate Behavior ◽

Processing Centre ◽

Olfactory Processing

AbstractAnimals can show either learned or innate behavioral responses to a given stimulus. How these circuits interact to produce an appropriate behavioral response is unknown. In the Drosophila olfactory system, the lateral horn (LH) and the mushroom body (MB) are thought to mediate innate and learned olfactory behavior respectively, although the function of the LH has not been directly tested. Here we identify two LH cell-types (PD2a1/b1) that receive input from an MB output neuron required for recall of aversive olfactory memories. In contrast to the model above we find that PD2a1/b1 are required for aversive memory retrieval. PD2a1/b1 activity is modulated by training, indicating that memory information is passed to the innate olfactory processing centre. We map the connectivity of PD2a1/b1 to other olfactory neurons with connectomic data. This provides a circuit mechanism by which learned and unlearned olfactory information can interact to produce appropriate behavior.

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