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1.
PLoS Genet ; 16(8): e1009003, 2020 08.
Artículo en Inglés | MEDLINE | ID: mdl-32866139

RESUMEN

Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila.


Asunto(s)
Receptor de Serotonina 5-HT1B/genética , Receptores de Serotonina 5-HT1/genética , Receptores de Serotonina 5-HT2/genética , Neuronas Serotoninérgicas/metabolismo , Serotonina/metabolismo , Animales , Ritmo Circadiano/genética , Proteínas de Drosophila/genética , Drosophila melanogaster/genética , Regulación de la Expresión Génica/genética , Interneuronas/metabolismo , Proteínas de la Membrana/genética , Proteínas del Tejido Nervioso/genética , Neurotransmisores/genética , Receptores de Serotonina/genética , Serotonina/genética , Percepción Visual/genética
2.
J Neurosci ; 40(33): 6309-6327, 2020 08 12.
Artículo en Inglés | MEDLINE | ID: mdl-32641403

RESUMEN

Serotonergic neurons project widely throughout the brain to modulate diverse physiological and behavioral processes. However, a single-cell resolution understanding of the connectivity of serotonergic neurons is currently lacking. Using a whole-brain EM dataset of a female Drosophila, we comprehensively determine the wiring logic of a broadly projecting serotonergic neuron (the CSDn) that spans several olfactory regions. Within the antennal lobe, the CSDn differentially innervates each glomerulus, yet surprisingly, this variability reflects a diverse set of presynaptic partners, rather than glomerulus-specific differences in synaptic output, which is predominately to local interneurons. Moreover, the CSDn has distinct connectivity relationships with specific local interneuron subtypes, suggesting that the CSDn influences distinct aspects of local network processing. Across olfactory regions, the CSDn has different patterns of connectivity, even having different connectivity with individual projection neurons that also span these regions. Whereas the CSDn targets inhibitory local neurons in the antennal lobe, the CSDn has more distributed connectivity in the LH, preferentially synapsing with principal neuron types based on transmitter content. Last, we identify individual novel synaptic partners associated with other sensory domains that provide strong, top-down input to the CSDn. Together, our study reveals the complex connectivity of serotonergic neurons, which combine the integration of local and extrinsic synaptic input in a nuanced, region-specific manner.SIGNIFICANCE STATEMENT All sensory systems receive serotonergic modulatory input. However, a comprehensive understanding of the synaptic connectivity of individual serotonergic neurons is lacking. In this study, we use a whole-brain EM microscopy dataset to comprehensively determine the wiring logic of a broadly projecting serotonergic neuron in the olfactory system of Drosophila Collectively, our study demonstrates, at a single-cell level, the complex connectivity of serotonergic neurons within their target networks, identifies specific cell classes heavily targeted for serotonergic modulation in the olfactory system, and reveals novel extrinsic neurons that provide strong input to this serotonergic system outside of the context of olfaction. Elucidating the connectivity logic of individual modulatory neurons provides a ground plan for the seemingly heterogeneous effects of modulatory systems.


Asunto(s)
Encéfalo/ultraestructura , Neuronas Serotoninérgicas/ultraestructura , Animales , Drosophila , Femenino , Vías Nerviosas/ultraestructura , Vías Olfatorias/ultraestructura , Sinapsis/ultraestructura
3.
Proc Natl Acad Sci U S A ; 115(21): 5588-5593, 2018 05 22.
Artículo en Inglés | MEDLINE | ID: mdl-29735707

RESUMEN

Nervous systems must distinguish sensory signals derived from an animal's own movements (reafference) from environmentally derived sources (exafference). To accomplish this, motor networks producing reafference transmit motor information, via a corollary discharge circuit (CDC), to affected sensory networks, modulating sensory function during behavior. While CDCs have been described in most sensory modalities, none have been observed projecting to an olfactory pathway. In moths, two mesothoracic to deutocerebral histaminergic neurons (MDHns) project from flight sensorimotor centers in the mesothoracic neuromere to the antennal lobe (AL), where they provide the sole source of histamine (HA), but whether they represent a CDC is unknown. We demonstrate that MDHn spiking activity is positively correlated with wing-motor output and increased before bouts of motor activity, suggesting that MDHns communicate global locomotor state, rather than providing a precisely timed motor copy. Within the AL, HA application sharpened entrainment of projection neuron responses to odor stimuli embedded within simulated wing-beat-induced flows, whereas MDHn axotomy or AL HA receptor (HA-r) blockade reduced entrainment. This finding is consistent with higher-order CDCs, as the MDHns enhanced rather than filtered entrainment of AL projection neurons. Finally, HA-r blockade increased odor detection and discrimination thresholds in behavior assays. These results establish MDHns as a CDC that modulates AL temporal resolution, enhancing odor-guided behavior. MDHns thus appear to represent a higher-order CDC to an insect olfactory pathway; this CDC's unique nature highlights the importance of motor-to-sensory signaling as a context-specific mechanism that fine-tunes sensory function.


Asunto(s)
Vuelo Animal , Histamina/farmacología , Vías Olfatorias/fisiología , Neuronas Receptoras Olfatorias/fisiología , Alas de Animales/fisiología , Animales , Manduca , Bulbo Olfatorio/citología , Bulbo Olfatorio/efectos de los fármacos , Bulbo Olfatorio/fisiología , Vías Olfatorias/efectos de los fármacos , Neuronas Receptoras Olfatorias/citología , Neuronas Receptoras Olfatorias/efectos de los fármacos , Alas de Animales/efectos de los fármacos
4.
J Neurophysiol ; 123(6): 2406-2425, 2020 06 01.
Artículo en Inglés | MEDLINE | ID: mdl-32401124

RESUMEN

The serotonergic system has been widely studied across animal taxa and different functional networks. This modulatory system is therefore well positioned to compare the consequences of neuromodulation for sensory processing across species and modalities at multiple levels of sensory organization. Serotonergic neurons that innervate sensory networks often bidirectionally exchange information with these networks but also receive input representative of motor events or motivational state. This convergence of information supports serotonin's capacity for contextualizing sensory information according to the animal's physiological state and external events. At the level of sensory circuitry, serotonin can have variable effects due to differential projections across specific sensory subregions, as well as differential serotonin receptor type expression within those subregions. Functionally, this infrastructure may gate or filter sensory inputs to emphasize specific stimulus features or select among different streams of information. The near-ubiquitous presence of serotonin and other neuromodulators within sensory regions, coupled with their strong effects on stimulus representation, suggests that these signaling pathways should be considered integral components of sensory systems.


Asunto(s)
Percepción Auditiva/fisiología , Red Nerviosa/fisiología , Percepción Olfatoria/fisiología , Receptores de Serotonina/metabolismo , Neuronas Serotoninérgicas/fisiología , Serotonina/metabolismo , Transducción de Señal/fisiología , Animales , Red Nerviosa/metabolismo , Neuronas Serotoninérgicas/metabolismo
5.
J Neurosci ; 37(31): 7318-7331, 2017 08 02.
Artículo en Inglés | MEDLINE | ID: mdl-28659283

RESUMEN

Modulatory neurons project widely throughout the brain, dynamically altering network processing based on an animal's physiological state. The connectivity of individual modulatory neurons can be complex, as they often receive input from a variety of sources and are diverse in their physiology, structure, and gene expression profiles. To establish basic principles about the connectivity of individual modulatory neurons, we examined a pair of identified neurons, the "contralaterally projecting, serotonin-immunoreactive deutocerebral neurons" (CSDns), within the olfactory system of Drosophila Specifically, we determined the neuronal classes providing synaptic input to the CSDns within the antennal lobe (AL), an olfactory network targeted by the CSDns, and the degree to which CSDn active zones are uniformly distributed across the AL. Using anatomical techniques, we found that the CSDns received glomerulus-specific input from olfactory receptor neurons (ORNs) and projection neurons (PNs), and networkwide input from local interneurons (LNs). Furthermore, we quantified the number of CSDn active zones in each glomerulus and found that CSDn output is not uniform, but rather heterogeneous, across glomeruli and stereotyped from animal to animal. Finally, we demonstrate that the CSDns synapse broadly onto LNs and PNs throughout the AL but do not synapse upon ORNs. Our results demonstrate that modulatory neurons do not necessarily provide purely top-down input but rather receive neuron class-specific input from the networks that they target, and that even a two cell modulatory network has highly heterogeneous, yet stereotyped, pattern of connectivity.SIGNIFICANCE STATEMENT Modulatory neurons often project broadly throughout the brain to alter processing based on physiological state. However, the connectivity of individual modulatory neurons to their target networks is not well understood, as modulatory neuron populations are heterogeneous in their physiology, morphology, and gene expression. In this study, we use a pair of identified serotonergic neurons within the Drosophila olfactory system as a model to establish a framework for modulatory neuron connectivity. We demonstrate that individual modulatory neurons can integrate neuron class-specific input from their target network, which is often nonreciprocal. Additionally, modulatory neuron output can be stereotyped, yet nonuniform, across network regions. Our results provide new insight into the synaptic relationships that underlie network function of modulatory neurons.


Asunto(s)
Drosophila/citología , Interneuronas/citología , Red Nerviosa/citología , Vías Olfatorias/citología , Neuronas Receptoras Olfatorias/citología , Neuronas Serotoninérgicas/citología , Sinapsis/ultraestructura , Animales , Conectoma , Drosophila/fisiología , Interneuronas/fisiología , Red Nerviosa/fisiología , Vías Olfatorias/fisiología , Neuronas Receptoras Olfatorias/fisiología , Neuronas Serotoninérgicas/fisiología , Olfato/fisiología , Sinapsis/fisiología , Transmisión Sináptica/fisiología
6.
Proc Biol Sci ; 284(1859)2017 Jul 26.
Artículo en Inglés | MEDLINE | ID: mdl-28747471

RESUMEN

Nervous systems must adapt to shifts in behavioural ecology. One form of adaptation is neural exaptation, in which neural circuits are co-opted to perform additional novel functions. Here, we describe the co-option of a motor-to-somatosensory circuit into an olfactory network. Many moths beat their wings during odour-tracking, whether walking or flying, causing strong oscillations of airflow around the antennae, altering odour plume structure. This self-induced sensory stimulation could impose selective pressures that influence neural circuit evolution, specifically fostering the emergence of corollary discharge circuits. In Manduca sexta, a pair of mesothoracic to deutocerebral histaminergic neurons (MDHns), project from the mesothoracic neuromere to both antennal lobes (ALs), the first olfactory neuropil. Consistent with a hypothetical role in providing the olfactory system with a corollary discharge, we demonstrate that the MDHns innervate the ALs of advanced and basal moths, but not butterflies, which differ in wing beat and flight pattern. The MDHns probably arose in crustaceans and in many arthropods innervate mechanosensory areas, but not the olfactory system. The MDHns, therefore, represent an example of architectural exaptation, in which neurons that provide motor output information to mechanosensory regions have been co-opted to provide information to the olfactory system in moths.


Asunto(s)
Vuelo Animal , Manduca/fisiología , Neuronas/fisiología , Bulbo Olfatorio/fisiología , Animales , Histamina , Olfato/fisiología , Alas de Animales
7.
Appl Environ Microbiol ; 82(9): 2644-55, 2016 May.
Artículo en Inglés | MEDLINE | ID: mdl-26896136

RESUMEN

Transmission, critical to the establishment and persistence of host-associated microbiotas, also exposes symbionts to new environmental conditions. With horizontal transmission, these different conditions represent major lifestyle shifts. Yet genome-wide analyses of how microbes adjust their transcriptomes toward these dramatic shifts remain understudied. Here, we provide a comprehensive and comparative analysis of the global transcriptional profiles of a symbiont as it shifts between lifestyles during transmission. The gammaproteobacterium Aeromonas veronii is transmitted from the gut of the medicinal leech to other hosts via host mucosal castings, yet A. veronii can also transition from mucosal habitancy to a free-living lifestyle. These three lifestyles are characterized by distinct physiological constraints and consequently lifestyle-specific changes in the expression of stress-response genes. Mucus-bound A. veronii had the greatest expression in terms of both the number of loci and levels of transcription of stress-response mechanisms. However, these bacteria are still capable of proliferating within the mucus, suggesting the availability of nutrients within this environment. We found that A. veronii alters transcription of loci in a synthetic pathway that obtains and incorporates N-acetylglucosamine (NAG; a major component of mucus) into the bacterial cell wall, enabling proliferation. Our results demonstrate that symbionts undergo dramatic local adaptation, demonstrated by widespread transcriptional changes, throughout the process of transmission that allows them to thrive while they encounter new environments which further shape their ecology and evolution.


Asunto(s)
Aeromonas veronii/metabolismo , Aeromonas veronii/fisiología , Sanguijuelas/microbiología , Moco/microbiología , Aeromonas veronii/genética , Aeromonas veronii/crecimiento & desarrollo , Animales , Evolución Biológica , ADN Bacteriano/genética , Ecología , Tracto Gastrointestinal/microbiología , Estudio de Asociación del Genoma Completo , Interacciones Huésped-Patógeno , Sanguijuelas/fisiología , Redes y Vías Metabólicas , Moco/metabolismo , Análisis de Secuencia de ADN , Simbiosis , Transcriptoma
8.
J Neurosci ; 33(9): 3786-98, 2013 Feb 27.
Artículo en Inglés | MEDLINE | ID: mdl-23447591

RESUMEN

Behavioral states often preferentially enhance specific classes of behavior and suppress incompatible behaviors. In the nervous system, this may involve upregulation of the efficacy of neural modules that mediate responses to one stimulus and suppression of modules that generate antagonistic or incompatible responses to another stimulus. In Aplysia, prestimulation of egestive inputs [esophageal nerve (EN)] facilitates subsequent EN-elicited egestive responses and weakens ingestive responses to ingestive inputs [Cerebral-Buccal Interneuron (CBI-2)]. However, a single state can also promote incompatible behaviors in response to different stimuli. This is the case in Aplysia, where prestimulation of CBI-2 inputs not only enhances subsequent CBI-2-elicited ingestive responses, but also strengthens EN-elicited egestive responses. We used the modularly organized feeding network of Aplysia to characterize the organizational principles that allow a single network state to promote two opposing behaviors, ingestion and egestion, without the two interfering with each other. We found that the CBI-2 prestimulation-induced state upregulates the excitability of neuron B65 which, as a member of the egestive module, increases the strength of egestive responses. Furthermore, we found that this upregulation is likely mediated by the actions of the neuropeptides FCAP (Feeding Circuit Activating Peptide) and CP2 (Cerebral Peptide 2). This increased excitability is mediated by a form of modulation that we refer to as "latent modulation" because it is established during stimulation of CBI-2, which does not activate B65. However, when B65 is recruited into EN-elicited egestive responses, the effects of the latent modulation are expressed as a higher B65 firing rate and a resultant strengthening of the egestive response.


Asunto(s)
Conducta Alimentaria/fisiología , Actividad Motora/fisiología , Red Nerviosa/citología , Red Nerviosa/fisiología , Neuronas/fisiología , Potenciales de Acción/efectos de los fármacos , Potenciales de Acción/fisiología , Análisis de Varianza , Animales , Aplysia/anatomía & histología , Aplysia/fisiología , Biofisica , Estimulación Eléctrica , Conducta Alimentaria/efectos de los fármacos , Potenciales Postsinápticos Inhibidores/fisiología , Vías Nerviosas/citología , Vías Nerviosas/fisiología , Neuronas/clasificación , Neuronas/efectos de los fármacos , Neuropéptidos/farmacología
9.
Biology (Basel) ; 13(2)2024 Feb 02.
Artículo en Inglés | MEDLINE | ID: mdl-38392312

RESUMEN

Neural networks have an extensive ability to change in response to environmental stimuli. This flexibility peaks during restricted windows of time early in life called critical periods. The ubiquitous occurrence of this form of plasticity across sensory modalities and phyla speaks to the importance of critical periods for proper neural development and function. Extensive investigation into visual critical periods has advanced our knowledge of the molecular events and key processes that underlie the impact of early-life experience on neuronal plasticity. However, despite the importance of olfaction for the overall survival of an organism, the cellular and molecular basis of olfactory critical periods have not garnered extensive study compared to visual critical periods. Recent work providing a comprehensive mapping of the highly organized olfactory neuropil and its development has in turn attracted a growing interest in how these circuits undergo plasticity during critical periods. Here, we perform a comparative review of olfactory critical periods in fruit flies and mice to provide novel insight into the importance of early odor exposure in shaping neural circuits and highlighting mechanisms found across sensory modalities.

10.
bioRxiv ; 2024 Apr 14.
Artículo en Inglés | MEDLINE | ID: mdl-38645269

RESUMEN

Serotonin (5-HT) is known to modulate early development during critical periods when experience drives heightened levels of plasticity in neurons. Here, we take advantage of the genetically tractable olfactory system of Drosophila to investigate how 5-HT modulates critical period plasticity in the CO2 sensing circuit of fruit flies. Our study reveals that 5HT modulation of multiple neuronal targets is necessary for experience-dependent structural changes in an odor processing circuit. The olfactory CPP is known to involve local inhibitory networks and consistent with this we found that knocking down 5-HT7 receptors in a subset of GABAergic local interneurons was sufficient to block CPP, as was knocking down GABA receptors expressed by olfactory sensory neurons (OSNs). Additionally, direct modulation of OSNs via 5-HT2B expression in the cognate OSNs sensing CO2 is also essential for CPP. Furthermore, 5-HT1B expression by serotonergic neurons in the olfactory system is also required during the critical period. Our study reveals that 5-HT modulation of multiple neuronal targets is necessary for experience-dependent structural changes in an odor processing circuit.

11.
Curr Biol ; 34(5): 1059-1075.e5, 2024 03 11.
Artículo en Inglés | MEDLINE | ID: mdl-38402616

RESUMEN

Natural behaviors are a coordinated symphony of motor acts that drive reafferent (self-induced) sensory activation. Individual sensors cannot disambiguate exafferent (externally induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to carry out adaptive behaviors through corollary discharge circuits (CDCs), which provide predictive motor signals from motor pathways to sensory processing and other motor pathways. Yet, how CDCs comprehensively integrate into the nervous system remains unexplored. Here, we use connectomics, neuroanatomical, physiological, and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs) in Drosophila, which function as a predictive CDC in other insects. Both AHN pairs receive input primarily from a partially overlapping population of descending neurons, especially from DNg02, which controls wing motor output. Using Ca2+ imaging and behavioral recordings, we show that AHN activation is correlated to flight behavior and precedes wing motion. Optogenetic activation of DNg02 is sufficient to activate AHNs, indicating that AHNs are activated by descending commands in advance of behavior and not as a consequence of sensory input. Downstream, each AHN pair targets predominantly non-overlapping networks, including those that process visual, auditory, and mechanosensory information, as well as networks controlling wing, haltere, and leg sensorimotor control. These results support the conclusion that the AHNs provide a predictive motor signal about wing motor state to mostly non-overlapping sensory and motor networks. Future work will determine how AHN signaling is driven by other descending neurons and interpreted by AHN downstream targets to maintain adaptive sensorimotor performance.


Asunto(s)
Drosophila , Neuronas , Animales , Drosophila/fisiología , Vías Eferentes , Insectos
12.
J Neurosci ; 32(49): 17740-52, 2012 Dec 05.
Artículo en Inglés | MEDLINE | ID: mdl-23223294

RESUMEN

Behavior is a product of both the stimuli encountered and the current internal state. At the level of the nervous system, the internal state alters the biophysical properties of, and connections between, neurons establishing a "network state." To establish a network state, the nervous system must be altered from an initial default/resting state, but what remains unclear is the extent to which this process represents induction from a passive default state or the removal of suppression by an active default state. We use repetition priming (a history-dependent improvement of behavioral responses to repeatedly encountered stimuli) to determine the cellular mechanisms underlying the transition from the default to the primed network state. We demonstrate that both removal of active suppression and induction of neuron excitability changes each contribute separately to the production of a primed state. The feeding system of Aplysia californica displays repetition priming via an increase in the activity of the radula closure neuron B8, which results in increased bite strength with each motor program. We found that during priming, B8 received progressively less inhibitory input from the multifunctional neurons B4/5. Additionally, priming enhanced the excitability of B8, but the rate at which B8 activity increased as a result of these changes was regulated by the progressive removal of inhibitory input. Thus, the establishment of the network state involves the induction of processes from a rested state, yet the consequences of these processes are conditional upon critical gating mechanisms actively enforced by the default state.


Asunto(s)
Neuronas Motoras/fisiología , Inhibición Neural/fisiología , Memoria Implícita/fisiología , Potenciales de Acción/fisiología , Animales , Aplysia , Estimulación Eléctrica/métodos , Conducta Alimentaria/fisiología , Interneuronas/fisiología , Boca/fisiología
13.
J Neurophysiol ; 109(9): 2327-34, 2013 May.
Artículo en Inglés | MEDLINE | ID: mdl-23407357

RESUMEN

Neurotransmitters can have diverse effects that occur over multiple time scales often making the consequences of neurotransmission difficult to predict. To explore the consequences of this diversity, we used the buccal ganglion of Aplysia to examine the effects of GABA release by a single interneuron, B40, on the intrinsic properties and motor output of the radula closure neuron B8. B40 induces a picrotoxin-sensitive fast IPSP lasting milliseconds in B8 and a slow EPSP lasting seconds. We found that the excitatory effects of this slow EPSP are also mediated by GABA. Together, these two GABAergic actions structure B8 firing in a pattern characteristic of ingestive programs. Furthermore, we found that repeated B40 stimulation induces a persistent increase in B8 excitability that was occluded in the presence of the GABA B receptor agonist baclofen, suggesting that GABA affects B8 excitability over multiple time scales. The phasing of B8 activity during the feeding motor programs determines the nature of the behavior elicited during that motor program. The persistent increase in B8 excitability induced by B40 biased the activity of B8 during feeding motor programs causing the motor programs to become more ingestive in nature. Thus, a single transmitter released from a single interneuron can have consequences for motor output that are expressed over multiple time scales. Importantly, despite the differences in their signs and temporal characteristics, the three actions of B40 are coherent in that they promote B8 firing patterns that are characteristic of ingestive motor outputs.


Asunto(s)
Potenciales Postsinápticos Excitadores , Interneuronas/fisiología , Actividad Motora , Ácido gamma-Aminobutírico/metabolismo , Animales , Aplysia , Baclofeno/farmacología , Ingestión de Alimentos , Conducta Alimentaria , Antagonistas del GABA/farmacología , Agonistas de Receptores GABA-B/farmacología , Neuronas GABAérgicas/efectos de los fármacos , Neuronas GABAérgicas/metabolismo , Neuronas GABAérgicas/fisiología , Ganglios de Invertebrados/citología , Ganglios de Invertebrados/fisiología , Interneuronas/efectos de los fármacos , Interneuronas/metabolismo , Picrotoxina/farmacología , Factores de Tiempo
14.
Nat Commun ; 14(1): 5280, 2023 08 30.
Artículo en Inglés | MEDLINE | ID: mdl-37644052

RESUMEN

Sensory systems are dynamically adjusted according to the animal's ongoing needs by neuromodulators, such as neuropeptides. Neuropeptides are often widely-distributed throughout sensory networks, but it is unclear whether such neuropeptides uniformly modulate network activity. Here, we leverage the Drosophila antennal lobe (AL) to resolve whether myoinhibitory peptide (MIP) uniformly modulates AL processing. Despite being uniformly distributed across the AL, MIP decreases olfactory input to some glomeruli, while increasing olfactory input to other glomeruli. We reveal that a heterogeneous ensemble of local interneurons (LNs) are the sole source of AL MIP, and show that differential expression of the inhibitory MIP receptor across glomeruli allows MIP to act on distinct intraglomerular substrates. Our findings demonstrate how even a seemingly simple case of modulation can have complex consequences on network processing by acting non-uniformly within different components of the overall network.


Asunto(s)
Drosophila , Olfato , Animales , Expresión Génica , Interneuronas
15.
bioRxiv ; 2023 Jun 09.
Artículo en Inglés | MEDLINE | ID: mdl-37333334

RESUMEN

Natural behaviors are a coordinated symphony of motor acts which drive self-induced or reafferent sensory activation. Single sensors only signal presence and magnitude of a sensory cue; they cannot disambiguate exafferent (externally-induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to make appropriate decisions and initiate adaptive behavioral outcomes. This is mediated by predictive motor signaling mechanisms, which emanate from motor control pathways to sensory processing pathways, but how predictive motor signaling circuits function at the cellular and synaptic level is poorly understood. We use a variety of techniques, including connectomics from both male and female electron microscopy volumes, transcriptomics, neuroanatomical, physiological and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs), which putatively provide predictive motor signals to several sensory and motor neuropil. Both AHN pairs receive input primarily from an overlapping population of descending neurons, many of which drive wing motor output. The two AHN pairs target almost exclusively non-overlapping downstream neural networks including those that process visual, auditory and mechanosensory information as well as networks coordinating wing, haltere, and leg motor output. These results support the conclusion that the AHN pairs multi-task, integrating a large amount of common input, then tile their output in the brain, providing predictive motor signals to non-overlapping sensory networks affecting motor control both directly and indirectly.

16.
J Neurophysiol ; 108(2): 539-50, 2012 Jul.
Artículo en Inglés | MEDLINE | ID: mdl-22552185

RESUMEN

The need to detect and process sensory cues varies in different behavioral contexts. Plasticity in sensory coding can be achieved by the context-specific release of neuromodulators in restricted brain areas. The context of aversion triggers the release of dopamine in the insect brain, yet the effects of dopamine on sensory coding are unknown. In this study, we characterize the morphology of dopaminergic neurons that innervate each of the antennal lobes (ALs; the first synaptic neuropils of the olfactory system) of the moth Manduca sexta and demonstrate with electrophysiology that dopamine enhances odor-evoked responses of the majority of AL neurons while reducing the responses of a small minority. Because dopamine release in higher brain areas mediates aversive learning we developed a naturalistic, ecologically inspired aversive learning paradigm in which an innately appetitive host plant floral odor is paired with a mimic of the aversive nectar of herbivorized host plants. This pairing resulted in a decrease in feeding behavior that was blocked when dopamine receptor antagonists were injected directly into the ALs. These results suggest that a transient dopaminergic enhancement of sensory output from the AL contributes to the formation of aversive memories. We propose a model of olfactory modulation in which specific contexts trigger the release of different neuromodulators in the AL to increase olfactory output to downstream areas of processing.


Asunto(s)
Reacción de Prevención/fisiología , Encéfalo/fisiología , Dopamina/metabolismo , Manduca/fisiología , Plasticidad Neuronal/fisiología , Bulbo Olfatorio/fisiología , Olfato/fisiología , Animales
17.
Chem Senses ; 36(2): 209-20, 2011 Jan.
Artículo en Inglés | MEDLINE | ID: mdl-21059697

RESUMEN

The structure of the brain is a consequence of selective pressures and the ancestral brain structures modified by those pressures. The Hymenoptera are one of the most behaviorally complex insect orders, and the olfactory system of honeybees (one of the most derived members) has been extensively studied. To understand the context in which the olfactory system of the Hymenoptera evolved, we performed a variety of immunocytochemical and anatomical labeling techniques on the antennal lobes (ALs) of one of its most primitive members, the sawflies, to provide a comparison between the honeybee and other insect model species. The olfactory receptor neurons project from the antennae to fill the entire glomerular volume but do not form distinct tracts as in the honeybee. Labeling of projection neurons revealed 5 output tracts similar to those in moths and immunolabeling for several transmitters revealed distinct populations of local interneurons and centrifugal neurons that were also similar to moths. There were, however, no histaminergic or dopaminergic AL neurons. The similarities between sawflies and moths suggest that along with the great radiation and increased complexity of behavioral repertoire of the Hymenoptera, there were extensive modifications of AL structure.


Asunto(s)
Antenas de Artrópodos/ultraestructura , Evolución Biológica , Himenópteros , Animales , Inmunohistoquímica , Estadios del Ciclo de Vida , Microscopía Confocal , Filogenia
18.
Artículo en Inglés | MEDLINE | ID: mdl-21286727

RESUMEN

Local interneurons (LNs) play important roles in shaping and modulating the activity of output neurons in primary olfactory centers. Here, we studied the morphological characteristics, odor responses, and neurotransmitter content of LNs in the antennal lobe (AL, the insect primary olfactory center) of the moth Manduca sexta. We found that most LNs are broadly tuned, with all LNs responding to at least one odorant. 70% of the odorants evoked a response, and 22% of the neurons responded to all the odorants tested. Some LNs showed excitatory (35%) or inhibitory (33%) responses only, while 33% of the neurons showed both excitatory and inhibitory responses, depending on the odorant. LNs that only showed inhibitory responses were the most responsive, with 78% of the odorants evoking a response. Neurons were morphologically diverse, with most LNs innervating almost all glomeruli and others innervating restricted portions of the AL. 61 and 39% of LNs were identified as GABA-immunoreactive (GABA-ir) and non-GABA-ir, respectively. We found no correlations between odor responses and GABA-ir, neither between morphology and GABA-ir. These results show that, as observed in other insects, LNs are diverse, which likely determines the complexity of the inhibitory network that regulates AL output.


Asunto(s)
Interneuronas/citología , Interneuronas/metabolismo , Manduca/citología , Manduca/metabolismo , Vías Olfatorias/citología , Vías Olfatorias/metabolismo , Animales , Inmunohistoquímica , Masculino , Microelectrodos , Odorantes , Vibrisas/inervación
19.
J Neurosci ; 29(32): 9987-99, 2009 Aug 12.
Artículo en Inglés | MEDLINE | ID: mdl-19675233

RESUMEN

Visual scenes comprise enormous amounts of information from which nervous systems extract behaviorally relevant cues. In most model systems, little is known about the transformation of visual information as it occurs along visual pathways. We examined how visual information is transformed physiologically as it is communicated from the eye to higher-order brain centers using bumblebees, which are known for their visual capabilities. We recorded intracellularly in vivo from 30 neurons in the central bumblebee brain (the lateral protocerebrum) and compared these neurons to 132 neurons from more distal areas along the visual pathway, namely the medulla and the lobula. In these three brain regions (medulla, lobula, and central brain), we examined correlations between the neurons' branching patterns and their responses primarily to color, but also to motion stimuli. Visual neurons projecting to the anterior central brain were generally color sensitive, while neurons projecting to the posterior central brain were predominantly motion sensitive. The temporal response properties differed significantly between these areas, with an increase in spike time precision across trials and a decrease in average reliable spiking as visual information processing progressed from the periphery to the central brain. These data suggest that neurons along the visual pathway to the central brain not only are segregated with regard to the physical features of the stimuli (e.g., color and motion), but also differ in the way they encode stimuli, possibly to allow for efficient parallel processing to occur.


Asunto(s)
Abejas/fisiología , Neuronas/fisiología , Percepción Visual/fisiología , Potenciales de Acción , Animales , Abejas/anatomía & histología , Encéfalo/anatomía & histología , Encéfalo/fisiología , Color , Potenciales Evocados Visuales , Bulbo Raquídeo/anatomía & histología , Bulbo Raquídeo/fisiología , Potenciales de la Membrana , Microelectrodos , Movimiento (Física) , Neuronas/citología , Estimulación Luminosa , Factores de Tiempo , Vías Visuales/anatomía & histología , Vías Visuales/fisiología
20.
Curr Biol ; 30(16): R932-R934, 2020 08 17.
Artículo en Inglés | MEDLINE | ID: mdl-32810451

RESUMEN

Aedes aegypti and Anopheles coluzzii mosquitoes exhibit diurnal and nocturnal behaviors, respectively. Baik et al. reveal the clock network architecture underlying each species' light preferences.


Asunto(s)
Aedes , Anopheles , Relojes Circadianos , Animales , Reacción de Prevención
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