Functional and Anatomical Specificity in a Higher Olfactory Centre

Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.

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Neurogenetic dissection of the Drosophila lateral horn reveals major outputs, diverse behavioural functions, and interactions with the mushroom body

eLife ◽

10.7554/elife.43079 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 44

Author(s):

Michael-John Dolan ◽

Shahar Frechter ◽

Alexander Shakeel Bates ◽

Chuntao Dan ◽

Paavo Huoviala ◽

...

Keyword(s):

Mushroom Body ◽

Cell Types ◽

Olfactory Cues ◽

Body Site ◽

Olfactory Behavior ◽

Gal4 Driver ◽

Sensory Stimuli ◽

Lateral Horn ◽

Functional Understanding ◽

Innate Behaviour

Animals exhibit innate behaviours to a variety of sensory stimuli including olfactory cues. In Drosophila, one higher olfactory centre, the lateral horn (LH), is implicated in innate behaviour. However, our structural and functional understanding of the LH is scant, in large part due to a lack of sparse neurogenetic tools for this region. We generate a collection of split-GAL4 driver lines providing genetic access to 82 LH cell types. We use these to create an anatomical and neurotransmitter map of the LH and link this to EM connectomics data. We find ~30% of LH projections converge with outputs from the mushroom body, site of olfactory learning and memory. Using optogenetic activation, we identify LH cell types that drive changes in valence behavior or specific locomotor programs. In summary, we have generated a resource for manipulating and mapping LH neurons, providing new insights into the circuit basis of innate and learned olfactory behavior.

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

Science Advances ◽

10.1126/sciadv.abd6900 ◽

2021 ◽

Vol 7 (1) ◽

pp. eabd6900

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 ◽

Appropriate Behavior ◽

State Dependent

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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Classification and genetic targeting of cell types in the primary taste and premotor center of the adult Drosophila brain

eLife ◽

10.7554/elife.71679 ◽

2021 ◽

Vol 10 ◽

Author(s):

Gabriella R Sterne ◽

Hideo Otsuna ◽

Barry J Dickson ◽

Kristin Scott

Keyword(s):

Sensory Processing ◽

Cell Types ◽

Brain Regions ◽

Projection Neurons ◽

Sensorimotor Transformations ◽

Drosophila Brain ◽

Genetic Targeting ◽

And Behavior ◽

Insight Into ◽

Adult Drosophila

Neural circuits carry out complex computations that allow animals to evaluate food, select mates, move toward attractive stimuli, and move away from threats. In insects, the subesophageal zone (SEZ) is a brain region that receives gustatory, pheromonal, and mechanosensory inputs and contributes to the control of diverse behaviors, including feeding, grooming, and locomotion. Despite its importance in sensorimotor transformations, the study of SEZ circuits has been hindered by limited knowledge of the underlying diversity of SEZ neurons. Here, we generate a collection of split-GAL4 lines that provides precise genetic targeting of 138 different SEZ cell types in adult D. melanogaster, comprising approximately one third of all SEZ neurons. We characterize the single cell anatomy of these neurons and find that they cluster by morphology into six supergroups that organize the SEZ into discrete anatomical domains. We find that the majority of local SEZ interneurons are not classically polarized, suggesting rich local processing, whereas SEZ projection neurons tend to be classically polarized, conveying information to a limited number of higher brain regions. This study provides insight into the anatomical organization of the SEZ and generates resources that will facilitate further study of SEZ neurons and their contributions to sensory processing and behavior.

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Classification and genetic targeting of cell types in the primary taste and premotor center of the Drosophila brain

10.1101/2021.08.06.455433 ◽

2021 ◽

Author(s):

Gabriella R Sterne ◽

Hideo Otsuna ◽

Barry J Dickson ◽

Kristin Scott

Keyword(s):

Sensory Processing ◽

Neural Circuits ◽

Cell Types ◽

Brain Regions ◽

Projection Neurons ◽

Sensorimotor Transformations ◽

Drosophila Brain ◽

Genetic Targeting ◽

And Behavior ◽

Insight Into

Neural circuits carry out complex computations that allow animals to evaluate food, select mates, move toward attractive stimuli, and move away from threats. In insects, the subesophageal zone (SEZ) is a brain region that receives gustatory, pheromonal, and mechanosensory inputs and contributes to the control of diverse behaviors, including feeding, grooming, and locomotion. Despite its importance in sensorimotor transformations, the study of SEZ circuits has been hindered by limited knowledge of the underlying diversity of SEZ neurons. Here, we generate a collection of split-GAL4 lines that provides precise genetic targeting of 138 different SEZ cell types in adult D. melanogaster, comprising approximately one third of all SEZ neurons. We characterize the single cell anatomy of these neurons and find that they cluster by morphology into six supergroups that organize the SEZ into discrete anatomical domains. We find that the majority of local SEZ interneurons are not classically polarized, suggesting rich local processing, whereas SEZ projection neurons tend to be classically polarized, conveying information to a limited number of higher brain regions. This study provides insight into the anatomical organization of the SEZ and generates resources that will facilitate further study of SEZ neurons and their contributions to sensory processing and behavior.

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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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Neurogenetic dissection of the Drosophila innate olfactory processing center

10.1101/404277 ◽

2018 ◽

Cited By ~ 3

Author(s):

Michael-John Dolan ◽

Shahar Frechter ◽

Alexander Shakeel Bates ◽

Chuntao Dan ◽

Paavo Huoviala ◽

...

Keyword(s):

Small Groups ◽

Mushroom Body ◽

Light And Electron Microscopy ◽

Cell Types ◽

Structure And Function ◽

Cell Type ◽

Gal4 Driver ◽

Sensory Stimuli ◽

Innate Behaviour ◽

And Function

AbstractAnimals exhibit innate behaviours in response to a variety of sensory stimuli such as olfactory cues. In Drosophila, a higher olfactory centre called the lateral horn (LH) is implicated in innate behaviour. However, our knowledge of the structure and function of the LH is scant, due to the lack of sparse neurogenetic tools for this brain region. Here we generate a collection of split-GAL4 driver lines providing genetic access to 82 LH cell-types. We identify the neurotransmitter and axo-dendritic polarity for each cell-type. Using these lines were create an anatomical map of the LH. We found that ∼30% of LH projections converge with outputs from the mushroom body, the site of olfactory learning and memory. Finally, using optogenetic activation of small groups of LH neurons. We identify cell-types that drive changes in either valence or specific motor programs, such as turning and locomotion. In summary we have generated a resource for manipulating and mapping LH neurons in both light and electron microscopy and generated insights into the anatomy and function of the LH.

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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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Parallel pathways for sound processing and functional connectivity among layer 5 and 6 auditory corticofugal neurons

eLife ◽

10.7554/elife.42974 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 13

Author(s):

Ross S Williamson ◽

Daniel B Polley

Keyword(s):

Functional Connectivity ◽

Sensory Processing ◽

Cell Types ◽

Projection Neurons ◽

Cortical Projection ◽

Response Latencies ◽

Sound Processing ◽

Downstream Targets ◽

Sustained Activity ◽

Fast Spiking

Cortical layers (L) 5 and 6 are populated by intermingled cell-types with distinct inputs and downstream targets. Here, we made optogenetically guided recordings from L5 corticofugal (CF) and L6 corticothalamic (CT) neurons in the auditory cortex of awake mice to discern differences in sensory processing and underlying patterns of functional connectivity. Whereas L5 CF neurons showed broad stimulus selectivity with sluggish response latencies and extended temporal non-linearities, L6 CTs exhibited sparse selectivity and rapid temporal processing. L5 CF spikes lagged behind neighboring units and imposed weak feedforward excitation within the local column. By contrast, L6 CT spikes drove robust and sustained activity, particularly in local fast-spiking interneurons. Our findings underscore a duality among sub-cortical projection neurons, where L5 CF units are canonical broadcast neurons that integrate sensory inputs for transmission to distributed downstream targets, while L6 CT neurons are positioned to regulate thalamocortical response gain and selectivity.

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Implication of the Sensory Environment in Children with Autism Spectrum Disorder: Perspectives from School

International Journal of Environmental Research and Public Health ◽

10.3390/ijerph18147670 ◽

2021 ◽

Vol 18 (14) ◽

pp. 7670

Author(s):

Ana Gentil-Gutiérrez ◽

José Luis Cuesta-Gómez ◽

Paula Rodríguez-Fernández ◽

Jerónimo Javier González-Bernal

Keyword(s):

Autism Spectrum Disorder ◽

Sensory Processing ◽

Children With Autism ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Sensory Profile ◽

School Factors ◽

Cross Sectional ◽

Sensory Stimuli ◽

Children With Asd

(1) Background: Children with Autism Spectrum Disorder (ASD) frequently have difficulties in processing sensory information, which is a limitation when participating in different contexts, such as school. The objective of the present study was to compare the sensory processing characteristics of children with ASD in the natural context of school through the perception of professionals in the field of education, in comparison with neurodevelopmental children (2) Methods: A cross-sectional descriptive study as conducted with study population consisting of children between three and ten years old, 36 of whom were diagnosed with ASD and attended the Autismo Burgos association; the remaining 24 had neurotypical development. The degree of response of the children to sensory stimuli at school was evaluated using the Sensory Profile-2 (SP-2) questionnaire in its school version, answered by the teachers. (3) Results: Statistically significant differences were found in sensory processing patterns (p = 0.001), in sensory systems (p = 0.001) and in school factors (p = 0.001). Children with ASD who obtained worse results. (4) Conclusions: Children with ASD are prone to present sensory alterations in different contexts, giving nonadapted behavioral and learning responses.

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