scholarly journals Long-range projection neurons in the taste circuit of Drosophila

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Heesoo Kim ◽  
Colleen Kirkhart ◽  
Kristin Scott
Keyword(s):  
Mushroom Body ◽  
Conditioned Aversion ◽  
Projection Neurons ◽  
Neural Pathways ◽  
Learning Centers ◽  
Feeding Behaviors ◽  
Learned Behavior ◽  
Learned Behaviors ◽  
Receptor Neurons ◽  
Lateral Protocerebrum

Taste compounds elicit innate feeding behaviors and act as rewards or punishments to entrain other cues. The neural pathways by which taste compounds influence innate and learned behaviors have not been resolved. Here, we identify three classes of taste projection neurons (TPNs) in Drosophila melanogaster distinguished by their morphology and taste selectivity. TPNs receive input from gustatory receptor neurons and respond selectively to sweet or bitter stimuli, demonstrating segregated processing of different taste modalities. Activation of TPNs influences innate feeding behavior, whereas inhibition has little effect, suggesting parallel pathways. Moreover, two TPN classes are absolutely required for conditioned taste aversion, a learned behavior. The TPNs essential for conditioned aversion project to the superior lateral protocerebrum (SLP) and convey taste information to mushroom body learning centers. These studies identify taste pathways from sensory detection to higher brain that influence innate behavior and are essential for learned responses to taste compounds.

scholarly journals Direct neural pathways convey distinct visual information to Drosophila mushroom bodies

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Katrin Vogt ◽  
Yoshinori Aso ◽  
Toshihide Hige ◽  
Stephan Knapek ◽  
Toshiharu Ichinose ◽  
...  
Keyword(s):  
Visual Information ◽  
Mushroom Body ◽  
Mushroom Bodies ◽  
Small Subset ◽  
Projection Neurons ◽  
Neural Pathways ◽  
Associative Memories ◽  
Visual Projection ◽  
Olfactory Input ◽  
Odor Representation

Previously, we demonstrated that visual and olfactory associative memories of Drosophila share mushroom body (MB) circuits (<xref ref-type="bibr" rid="bib46">Vogt et al., 2014</xref>). Unlike for odor representation, the MB circuit for visual information has not been characterized. Here, we show that a small subset of MB Kenyon cells (KCs) selectively responds to visual but not olfactory stimulation. The dendrites of these atypical KCs form a ventral accessory calyx (vAC), distinct from the main calyx that receives olfactory input. We identified two types of visual projection neurons (VPNs) directly connecting the optic lobes and the vAC. Strikingly, these VPNs are differentially required for visual memories of color and brightness. The segregation of visual and olfactory domains in the MB allows independent processing of distinct sensory memories and may be a conserved form of sensory representations among insects.

Olfactory Representations by Drosophila Mushroom Body Neurons

2008 ◽  
Vol 99 (2) ◽  
pp. 734-746 ◽  
Author(s):  
Glenn C. Turner ◽  
Maxim Bazhenov ◽  
Gilles Laurent
Keyword(s):  
Olfactory Receptor ◽  
Mushroom Body ◽  
Temporal Integration ◽  
Activity Patterns ◽  
Olfactory Receptor Neurons ◽  
Projection Neurons ◽  
Contributing Factors ◽  
Receptor Neurons ◽  
Whole Cell Recordings

Learning and memory has been studied extensively in Drosophila using behavioral, molecular, and genetic approaches. These studies have identified the mushroom body as essential for the formation and retrieval of olfactory memories. We investigated odor responses of the principal neurons of the mushroom body, the Kenyon cells (KCs), in Drosophila using whole cell recordings in vivo. KC responses to odors were highly selective and, thus sparse, compared with those of their direct inputs, the antennal lobe projection neurons (PNs). We examined the mechanisms that might underlie this transformation and identified at least three contributing factors: excitatory synaptic potentials (from PNs) decay rapidly, curtailing temporal integration, PN convergence onto individual KCs is low (∼10 PNs per KC on average), and KC firing thresholds are high. Sparse activity is thought to be useful in structures involved in memory in part because sparseness tends to reduce representation overlaps. By comparing activity patterns evoked by the same odors across olfactory receptor neurons and across KCs, we show that representations of different odors do indeed become less correlated as they progress through the olfactory system.

scholarly journals Dissecting neural pathways for forgetting in Drosophila olfactory aversive memory

2015 ◽  
Vol 112 (48) ◽  
pp. E6663-E6672 ◽  
Author(s):  
Yichun Shuai ◽  
Areekul Hirokawa ◽  
Yulian Ai ◽  
Min Zhang ◽  
Wanhe Li ◽  
...  
Keyword(s):  
Reversal Learning ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Biologically Active ◽  
Molecular Pathways ◽  
Neural Pathways ◽  
Active Process ◽  
Glutamatergic Neurons ◽  
Memory Decay ◽  
Over Time

Recent studies have identified molecular pathways driving forgetting and supported the notion that forgetting is a biologically active process. The circuit mechanisms of forgetting, however, remain largely unknown. Here we report two sets of Drosophila neurons that account for the rapid forgetting of early olfactory aversive memory. We show that inactivating these neurons inhibits memory decay without altering learning, whereas activating them promotes forgetting. These neurons, including a cluster of dopaminergic neurons (PAM-β′1) and a pair of glutamatergic neurons (MBON-γ4>γ1γ2), terminate in distinct subdomains in the mushroom body and represent parallel neural pathways for regulating forgetting. Interestingly, although activity of these neurons is required for memory decay over time, they are not required for acute forgetting during reversal learning. Our results thus not only establish the presence of multiple neural pathways for forgetting in Drosophila but also suggest the existence of diverse circuit mechanisms of forgetting in different contexts.

scholarly journals An Avian Basal Ganglia-Forebrain Circuit Contributes Differentially to Syllable Versus Sequence Variability of Adult Bengalese Finch Song

2009 ◽  
Vol 101 (6) ◽  
pp. 3235-3245 ◽  
Author(s):  
Cara M. Hampton ◽  
Jon T. Sakata ◽  
Michael S. Brainard
Keyword(s):  
Basal Ganglia ◽  
Syllable Structure ◽  
Skill Learning ◽  
Behavioral Variability ◽  
Neural Pathways ◽  
Sequence Variability ◽  
Social Modulation ◽  
The Social ◽  
Learned Behaviors ◽  
Magnocellular Nucleus

Behavioral variability is important for motor skill learning but continues to be present and actively regulated even in well-learned behaviors. In adult songbirds, two types of song variability can persist and are modulated by social context: variability in syllable structure and variability in syllable sequencing. The degree to which the control of both types of adult variability is shared or distinct remains unknown. The output of a basal ganglia-forebrain circuit, LMAN (the lateral magnocellular nucleus of the anterior nidopallium), has been implicated in song variability. For example, in adult zebra finches, neurons in LMAN actively control the variability of syllable structure. It is unclear, however, whether LMAN contributes to variability in adult syllable sequencing because sequence variability in adult zebra finch song is minimal. In contrast, Bengalese finches retain variability in both syllable structure and syllable sequencing into adulthood. We analyzed the effects of LMAN lesions on the variability of syllable structure and sequencing and on the social modulation of these forms of variability in adult Bengalese finches. We found that lesions of LMAN significantly reduced the variability of syllable structure but not of syllable sequencing. We also found that LMAN lesions eliminated the social modulation of the variability of syllable structure but did not detect significant effects on the modulation of sequence variability. These results show that LMAN contributes differentially to syllable versus sequence variability of adult song and suggest that these forms of variability are regulated by distinct neural pathways.

scholarly journals Divergent neural pathways emanating from the lateral parabrachial nucleus mediate distinct components of the pain response

2019 ◽  
Author(s):  
Michael C. Chiang ◽  
Eileen K. Nguyen ◽  
Andrew E. Papale ◽  
Sarah E. Ross
Keyword(s):  
Ventromedial Hypothalamus ◽  
Parabrachial Nucleus ◽  
Projection Neurons ◽  
Pain Response ◽  
Neural Pathways ◽  
Bed Nucleus ◽  
Lateral Parabrachial Nucleus ◽  
Efferent Projections ◽  
Efferent Neurons ◽  
Nociceptive Input

ABSTRACTThe lateral parabrachial nucleus (lPBN) is a major target of spinal projection neurons conveying nociceptive input into supraspinal structures. However, the functional role of distinct lPBN efferents for diverse nocifensive responses have remained largely uncharacterized. Here, we show that two populations of efferent neurons from different regions of the lPBN collateralize to distinct targets. Activation of efferent projections to the ventromedial hypothalamus (VMH) or lateral periaqueductal gray (lPAG) drive escape behaviors, whereas the activation of lPBN efferents to the bed nucleus stria terminalis (BNST) or central amygdala (CEA) generates an aversive memory. Finally, we provide evidence that dynorphin expressing neurons span cytoarchitecturally distinct domains of the lPBN to coordinate these distinct aspects of the nocifensive response.HIGHLIGHTSSpatially segregated neurons in the lPBN collateralize to distinct targets.Distinct output pathways give rise to separate aspects of the pain response.Dynorphin neurons within the lPBN convey noxious information across subdivisions.eTOC BLURBChiang et al. reveal that neurons in spatially segregated regions of the lateral parabrachial nucleus collateralize to distinct targets, and that activation of distinct efferents gives rise to separate components of the nocifensive response.

scholarly journals Fronto-striatal projections regulate approach-avoidance conflict

2020 ◽  
Author(s):  
Adrienne C. Loewke ◽  
Adelaide R. Minerva ◽  
Alexandra B. Nelson ◽  
Anatol C. Kreitzer ◽  
Lisa A. Gunaydin
Keyword(s):  
Anxiety Disorders ◽  
Avoidance Behavior ◽  
D1 Receptor ◽  
Projection Neurons ◽  
Medium Spiny Neurons ◽  
Neural Pathways ◽  
Spiny Neurons ◽  
Striatal Projection Neurons ◽  
Neural Computations ◽  
Approach Avoidance

ABSTRACTThe dorsomedial prefrontal cortex (dmPFC) has been linked to approach-avoidance behavior and decision-making under conflict, key neural computations thought to be altered in anxiety disorders. However, the heterogeneity of efferent prefrontal projections has obscured identification of the specific top-down neural pathways regulating these anxiety-related behaviors. While the dmPFC-amygdala circuit has long been implicated in controlling reflexive fear responses, recent work suggests that this circuit is less important for avoidance behavior. We hypothesized that dmPFC neurons projecting to the dorsomedial striatum (DMS) represent a subset of prefrontal neurons that robustly encode and drive approach-avoidance behavior. Using fiber photometry recording during the elevated zero maze (EZM) task, we show heightened neural activity in prefrontal and fronto-striatal projection neurons, but not fronto-amydalar projection neurons, during exploration of the anxiogenic open arms of the maze. Additionally, through pathway-specific optogenetics we demonstrate that this fronto-striatal projection preferentially excites postsynaptic D1 receptor-expressing medium spiny neurons in the DMS and bidirectionally controls avoidance behavior. We conclude that this striatal-projecting subpopulation of prefrontal neurons regulates approach-avoidance conflict, supporting a model for prefrontal control of defensive behavior in which the dmPFC-amygdala projection controls reflexive fear behavior and the dmPFC-striatum projection controls anxious avoidance behavior. Our findings identify this fronto-striatal circuit as a valuable therapeutic target for developing interventions to alleviate excessive avoidance behavior in anxiety disorders.

scholarly journals Connectivity patterns shape sensory representation in a cerebellum-like network

2021 ◽  
Author(s):  
Daniel Zavitz ◽  
Elom A. Amematsro ◽  
Alla Borisyuk ◽  
Sophie J.C. Caron
Keyword(s):  
Learning Outcomes ◽  
Network Architecture ◽  
Mushroom Body ◽  
Structural Features ◽  
Projection Neurons ◽  
Sensory Representation ◽  
Learning Function ◽  
Kenyon Cells ◽  
Connectivity Patterns ◽  
Function Relationship

SUMMARYCerebellum-like structures are found in many brains and share a basic fan-out–fan-in network architecture. How the specific structural features of these networks give rise to their learning function remains largely unknown. To investigate this structure–function relationship, we developed a realistic computational model of an empirically very well-characterized cerebellum-like structure, the Drosophila melanogaster mushroom body. We show how well-defined connectivity patterns between the Kenyon cells, the constituent neurons of the mushroom body, and their input projection neurons enable different functions. First, biases in the likelihoods at which individual projection neurons connect to Kenyon cells allow the mushroom body to prioritize the learning of particular, ethologically meaningful odors. Second, groups of projection neurons connecting preferentially to the same Kenyon cells facilitate the mushroom body generalizing across similar odors. Altogether, our results demonstrate how different connectivity patterns shape the representation space of a cerebellum-like network and impact its learning outcomes.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

2021 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
Andre Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

scholarly journals Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

2020 ◽  
Author(s):  
Lothar Baltruschat ◽  
Philipp Ranft ◽  
Luigi Prisco ◽  
J. Scott Lauritzen ◽  
André Fiala ◽  
...  
Keyword(s):  
Conditioned Stimulus ◽  
Memory Consolidation ◽  
Mushroom Body ◽  
Structural Changes ◽  
De Novo ◽  
Projection Neurons ◽  
Structural Modifications ◽  
Behavioural Experiments ◽  
The Individual ◽  
Mushroom Body Calyx

SummaryThe capacity of utilizing past experience to guide future action is a fundamental and conserved function of the nervous system. Associative memory formation initiated by the coincident detection of a conditioned stimulus (CS, e.g. odour) and an unconditioned stimulus (US, e.g. sugar reward) can lead to a short-lived memory trace (STM) within distinct circuits [1-5]. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on de-novo protein synthesis [6, 7], require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones [8-17]. Compared to modulation of existing connections, the reorganization of circuits affords the unique possibility of sampling for potential new partners [18-20]. Nonetheless, only few examples of rewiring associated with learning have been established thus far [14, 21-24]. Here, we report that memory consolidation is associated with the structural and functional reorganization of an identified circuit in the adult fly brain. The formation and retrieval of olfactory associative memories in Drosophila requires the mushroom body (MB) [25]. We identified the individual synapses of olfactory projection neurons (PNs) that deliver a conditioned odour to the MB and reconstructed the complexity of the microcircuit they form. Combining behavioural experiments with high-resolution microscopy and functional imaging, we demonstrated that the consolidation of appetitive olfactory memories closely correlates with an increase in the number of synaptic complexes formed by the PNs that deliver the conditioned stimulus and their postsynaptic partners. These structural changes result in additional functional synaptic connections.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
André Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

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