scholarly journals Functional and anatomical specificity in a higher olfactory centre

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Shahar Frechter ◽  
Alexander Shakeel Bates ◽  
Sina Tootoonian ◽  
Michael-John Dolan ◽  
James Manton ◽  
...  
Keyword(s):  
Olfactory System ◽  
Mushroom Body ◽  
Cell Types ◽  
Sensory Systems ◽  
Projection Neurons ◽  
Olfactory Behavior ◽  
Population Code ◽  
Odor Coding ◽  
Sensory Stimuli ◽  
Lateral Horn

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.

scholarly journals Functional and Anatomical Specificity in a Higher Olfactory Centre

2018 ◽  
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.

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

eLife ◽  
2019 ◽  
Vol 8 ◽  
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.

scholarly journals Olfactory processing in the lateral horn of Drosophila

2021 ◽  
Vol 383 (1) ◽  
pp. 113-123
Author(s):  
Sudeshna Das Chakraborty ◽  
Silke Sachse
Keyword(s):  
Functional Properties ◽  
Olfactory System ◽  
Cell Types ◽  
Specific Cell ◽  
Olfactory Behavior ◽  
Lateral Horn ◽  
Behavioral Decision ◽  
Animal Phyla ◽  
Survival And Reproduction ◽  
Almost All

AbstractSensing olfactory signals in the environment represents a crucial and significant task of sensory systems in almost all organisms to facilitate survival and reproduction. Notably, the olfactory system of diverse animal phyla shares astonishingly many fundamental principles with regard to anatomical and functional properties. Binding of odor ligands by chemosensory receptors present in the olfactory peripheral organs leads to a neuronal activity that is conveyed to first and higher-order brain centers leading to a subsequent odor-guided behavioral decision. One of the key centers for integrating and processing innate olfactory behavior is the lateral horn (LH) of the protocerebrum in insects. In recent years the LH of Drosophila has garnered increasing attention and many studies have been dedicated to elucidate its circuitry. In this review we will summarize the recent advances in mapping and characterizing LH-specific cell types, their functional properties with respect to odor tuning, their neurotransmitter profiles, their connectivity to pre-synaptic and post-synaptic partner neurons as well as their impact for olfactory behavior as known so far.

scholarly journals Information flow, cell types and stereotypy in a full olfactory connectome

2020 ◽  
Author(s):  
Philipp Schlegel ◽  
Alexander Shakeel Bates ◽  
Tomke Stürner ◽  
Sridhar R. Jagannathan ◽  
Nikolas Drummond ◽  
...  
Keyword(s):  
Information Flow ◽  
Olfactory System ◽  
Mushroom Body ◽  
Antennal Lobe ◽  
Large Scale ◽  
Cell Types ◽  
Neuronal Morphology ◽  
Striking Similarity ◽  
Data Set ◽  
Lateral Horn

AbstractThe hemibrain connectome (Scheffer et al., 2020) provides large scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the most complex olfactory system studied at synaptic resolution to date, covering all first, second and third-order neurons of the olfactory system associated with the antennal lobe and lateral horn (mushroom body neurons are described in a parallel paper, (Li et al., 2020)). We develop a generally applicable strategy to extract information flow and layered organisation from synaptic resolution connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. We also leverage a second data set (FAFB, (Zheng et al., 2018)) to provide a first quantitative assessment of inter- versus intra-individual stereotypy. Complete reconstruction of select developmental lineages in two brains (three brain hemispheres) reveals striking similarity in neuronal morphology across brains for >170 cell types. Within and across brains, connectivity correlates with morphology. Notably, neurons of the same morphological type show similar connection variability within one brain as across brains; this property should enable a rigorous quantitative approach to cell typing.

scholarly journals Complete connectomic reconstruction of olfactory projection neurons in the fly brain

2020 ◽  
Author(s):  
A.S. Bates ◽  
P. Schlegel ◽  
R.J.V. Roberts ◽  
N. Drummond ◽  
I.F.M. Tamimi ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Olfactory System ◽  
Neuronal Cell ◽  
Building Blocks ◽  
Cell Types ◽  
Projection Neuron ◽  
Brain Regions ◽  
Projection Neurons ◽  
List Type ◽  
Lateral Horn

AbstractNervous systems contain sensory neurons, local neurons, projection neurons and motor neurons. To understand how these building blocks form whole circuits, we must distil these broad classes into neuronal cell types and describe their network connectivity. Using an electron micrograph dataset for an entire Drosophila melanogaster brain, we reconstruct the first complete inventory of olfactory projections connecting the antennal lobe, the insect analogue of the mammalian olfactory bulb, to higher-order brain regions in an adult animal brain. We then connect this inventory to extant data in the literature, providing synaptic-resolution ‘holotypes’ both for heavily investigated and previously unknown cell types. Projection neurons are approximately twice as numerous as reported by light level studies; cell types are stereotyped, but not identical, in cell and synapse numbers between brain hemispheres. The lateral horn, the insect analogue of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behaviour. Here, we find new connectivity motifs, including: axo-axonic connectivity between projection neurons; feedback and lateral inhibition of these axons by local neurons; and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto lateral horn neurons. This differs from the configuration of the second most prominent target for olfactory projection neurons: the mushroom body calyx, the insect analogue of the mammalian piriform cortex and a centre for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system.HighlightsFirst complete parts list for second-order neurons of an adult olfactory systemQuantification of left-right stereotypy in cell and synapse numberAxo-axonic connections form hierarchical communities in the lateral hornLocal neurons and memory-related feedback target projection neuron axons

scholarly journals Higher-order olfactory neurons in the lateral horn supports odor valence and odor identity coding in Drosophila

2021 ◽  
Author(s):  
Sudeshna Das Chakraborty ◽  
Hetan Chang ◽  
Bill S. Hansson ◽  
Silke Sachse
Keyword(s):  
Specific Activity ◽  
Excitatory Input ◽  
Higher Order ◽  
Second Order ◽  
Projection Neurons ◽  
Sensory Level ◽  
Specific Response ◽  
Response Patterns ◽  
Odor Coding ◽  
Lateral Horn

AbstractUnderstanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster. We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We found that odors evoke reproducible, stereotypic and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons.

scholarly journals Neurogenetic dissection of the Drosophila innate olfactory processing center

2018 ◽  
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.

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

2017 ◽  
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.

scholarly journals Connectivity characterization of the mouse basolateral amygdalar complex

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Houri Hintiryan ◽  
Ian Bowman ◽  
David L. Johnson ◽  
Laura Korobkova ◽  
Muye Zhu ◽  
...  
Keyword(s):  
Granular Cell ◽  
Cell Types ◽  
Projection Neurons ◽  
Cell Type ◽  
Connectivity Map ◽  
Analysis Techniques ◽  
Domain Specific ◽  
Cell Type Specific ◽  
Unique Domain

AbstractThe basolateral amygdalar complex (BLA) is implicated in behaviors ranging from fear acquisition to addiction. Optogenetic methods have enabled the association of circuit-specific functions to uniquely connected BLA cell types. Thus, a systematic and detailed connectivity profile of BLA projection neurons to inform granular, cell type-specific interrogations is warranted. Here, we apply machine-learning based computational and informatics analysis techniques to the results of circuit-tracing experiments to create a foundational, comprehensive BLA connectivity map. The analyses identify three distinct domains within the anterior BLA (BLAa) that house target-specific projection neurons with distinguishable morphological features. We identify brain-wide targets of projection neurons in the three BLAa domains, as well as in the posterior BLA, ventral BLA, posterior basomedial, and lateral amygdalar nuclei. Inputs to each nucleus also are identified via retrograde tracing. The data suggests that connectionally unique, domain-specific BLAa neurons are associated with distinct behavior networks.

scholarly journals A selective projection from the subthalamic nucleus to parvalbumin-expressing interneurons of the striatum

2020 ◽  
Author(s):  
Krishnakanth Kondabolu ◽  
Natalie M. Doig ◽  
Olaoluwa Ayeko ◽  
Bakhtawer Khan ◽  
Alexandra Torres ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Subthalamic Nucleus ◽  
Ex Vivo ◽  
Cell Types ◽  
Projection Neurons ◽  
Striatal Neurons ◽  
Primary Input ◽  
Cholinergic Interneurons ◽  
Axonal Connections ◽  
Excitatory Responses

AbstractThe striatum and subthalamic nucleus (STN) are considered to be the primary input nuclei of the basal ganglia. Projection neurons of both striatum and STN can extensively interact with other basal ganglia nuclei, and there is growing anatomical evidence of direct axonal connections from the STN to striatum. There remains, however, a pressing need to elucidate the organization and impact of these subthalamostriatal projections in the context of the diverse cell types constituting the striatum. To address this, we carried out monosynaptic retrograde tracing from genetically-defined populations of dorsal striatal neurons in adult male and female mice, quantifying the connectivity from STN neurons to spiny projection neurons, GABAergic interneurons, and cholinergic interneurons. In parallel, we used a combination of ex vivo electrophysiology and optogenetics to characterize the responses of a complementary range of dorsal striatal neuron types to activation of STN axons. Our tracing studies showed that the connectivity from STN neurons to striatal parvalbumin-expressing interneurons is significantly higher (~ four-to eight-fold) than that from STN to any of the four other striatal cell types examined. In agreement, our recording experiments showed that parvalbumin-expressing interneurons, but not the other cell types tested, commonly exhibited robust monosynaptic excitatory responses to subthalamostriatal inputs. Taken together, our data collectively demonstrate that the subthalamostriatal projection is highly selective for target cell type. We conclude that glutamatergic STN neurons are positioned to directly and powerfully influence striatal activity dynamics by virtue of their enriched innervation of GABAergic parvalbumin-expressing interneurons.

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