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1.
J Neurophysiol ; 131(3): 509-515, 2024 Mar 01.
Artigo em Inglês | MEDLINE | ID: mdl-38264774

RESUMO

Nervous systems have evolved to function consistently in the face of the normal environmental fluctuations experienced by animals. The stomatogastric nervous system (STNS) of the crab, Cancer borealis, produces a motor output that has been studied for its remarkable robustness in response to single global perturbations. Changes in environments, however, are often complex and multifactorial. Therefore, we studied the robustness of the pyloric network in the stomatogastric ganglion (STG) in response to simultaneous perturbations of temperature and pH. We compared the effects of elevated temperatures on the pyloric rhythm at control, acid, or base pHs. In each pH recordings were made at 11°C, and then the temperature was increased until the rhythms became disorganized ("crashed"). Pyloric burst frequencies and phase relationships showed minor differences between pH groups until reaching close to the crash temperatures. However, the temperatures at which the rhythms were disrupted were lower in the two extreme pH conditions. This indicates that one environmental stress can make an animal less resilient to a second stressor.NEW & NOTEWORTHY Resilience to environmental fluctuations is important for all animals. It is common that animals encounter multiple stressful events at the same time, the cumulative impacts of which are largely unknown. This study examines the effects of temperature and pH on the nervous system of crabs that live in the fluctuating environments of the Northern Atlantic Ocean. The ranges of tolerance to one perturbation, temperature, are reduced under the influence of a second, pH.


Assuntos
Braquiúros , Piloro , Animais , Temperatura , Piloro/fisiologia , Gânglios dos Invertebrados/fisiologia , Braquiúros/fisiologia
2.
J Neurophysiol ; 131(2): 417-434, 2024 Feb 01.
Artigo em Inglês | MEDLINE | ID: mdl-38197163

RESUMO

Network flexibility is important for adaptable behaviors. This includes neuronal switching, where neurons alter their network participation, including changing from single- to dual-network activity. Understanding the implications of neuronal switching requires determining how a switching neuron interacts with each of its networks. Here, we tested 1) whether "home" and second networks, operating via divergent rhythm generation mechanisms, regulate a switching neuron and 2) if a switching neuron, recruited via modulation of intrinsic properties, contributes to rhythm or pattern generation in a new network. Small, well-characterized feeding-related networks (pyloric, ∼1 Hz; gastric mill, ∼0.1 Hz) and identified modulatory inputs make the isolated crab (Cancer borealis) stomatogastric nervous system (STNS) a useful model to study neuronal switching. In particular, the neuropeptide Gly1-SIFamide switches the lateral posterior gastric (LPG) neuron (2 copies) from pyloric-only to dual-frequency pyloric/gastric mill (fast/slow) activity via modulation of LPG-intrinsic properties. Using current injections to manipulate neuronal activity, we found that gastric mill, but not pyloric, network neurons regulated the intrinsically generated LPG slow bursting. Conversely, selective elimination of LPG from both networks using photoinactivation revealed that LPG regulated gastric mill neuron-firing frequencies but was not necessary for gastric mill rhythm generation or coordination. However, LPG alone was sufficient to produce a distinct pattern of network coordination. Thus, modulated intrinsic properties underlying dual-network participation may constrain which networks can regulate switching neuron activity. Furthermore, recruitment via intrinsic properties may occur in modulatory states where it is important for the switching neuron to actively contribute to network output.NEW & NOTEWORTHY We used small, well-characterized networks to investigate interactions between rhythmic networks and neurons that switch their network participation. For a neuron switching into dual-network activity, only the second network regulated its activity in that network. In addition, the switching neuron was sufficient but not necessary to coordinate second network neurons and regulated their activity levels. Thus, regulation of switching neurons may be selective, and a switching neuron is not necessarily simply a follower in additional networks.


Assuntos
Braquiúros , Neurônios , Animais , Neurônios/fisiologia , Piloro/fisiologia , Braquiúros/fisiologia , Gânglios dos Invertebrados/fisiologia , Periodicidade , Rede Nervosa/fisiologia
3.
J Neurosci ; 44(1)2024 Jan 03.
Artigo em Inglês | MEDLINE | ID: mdl-37968117

RESUMO

Neuromodulation lends flexibility to neural circuit operation but the general notion that different neuromodulators sculpt neural circuit activity into distinct and characteristic patterns is complicated by interindividual variability. In addition, some neuromodulators converge onto the same signaling pathways, with similar effects on neurons and synapses. We compared the effects of three neuropeptides on the rhythmic pyloric circuit in the stomatogastric ganglion of male crabs, Cancer borealis Proctolin (PROC), crustacean cardioactive peptide (CCAP), and red pigment concentrating hormone (RPCH) activate the same modulatory inward current, I MI, and have convergent actions on synapses. However, while PROC targets all four neuron types in the core pyloric circuit, CCAP and RPCH target the same subset of only two neurons. After removal of spontaneous neuromodulator release, none of the neuropeptides restored the control cycle frequency, but all restored the relative timing between neuron types. Consequently, differences between neuropeptide effects were mainly found in the spiking activity of different neuron types. We performed statistical comparisons using the Euclidean distance in the multidimensional space of normalized output attributes to obtain a single measure of difference between modulatory states. Across preparations, the circuit output in PROC was distinguishable from CCAP and RPCH, but CCAP and RPCH were not distinguishable from each other. However, we argue that even between PROC and the other two neuropeptides, population data overlapped enough to prevent reliable identification of individual output patterns as characteristic for a specific neuropeptide. We confirmed this notion by showing that blind classifications by machine learning algorithms were only moderately successful.Significance Statement It is commonly assumed that distinct behaviors or circuit activities can be elicited by different neuromodulators. Yet it is unknown to what extent these characteristic actions remain distinct across individuals. We use a well-studied circuit model of neuromodulation to examine the effects of three neuropeptides, each known to produce a distinct activity pattern in controlled studies. We find that, when compared across individuals, the three peptides elicit activity patterns that are either statistically indistinguishable or show too much overlap to be labeled characteristic. We ascribe this to interindividual variability and overlapping subcellular actions of the modulators. Because both factors are common in all neural circuits, these findings have broad significance for understanding chemical neuromodulatory actions while considering interindividual variability.


Assuntos
Braquiúros , Neuropeptídeos , Masculino , Humanos , Animais , Neuropeptídeos/metabolismo , Peptídeos/farmacologia , Neurônios/fisiologia , Neurotransmissores/farmacologia , Transdução de Sinais , Braquiúros/fisiologia , Gânglios dos Invertebrados/fisiologia
4.
J Neurophysiol ; 130(4): 941-952, 2023 10 01.
Artigo em Inglês | MEDLINE | ID: mdl-37671445

RESUMO

Command systems integrate sensory information and then activate the interneurons and motor neurons that mediate behavior. Much research has established that the higher-order projection neurons that constitute these systems can play a key role in specifying the nature of the motor activity induced, or determining its parametric features. To a large extent, these insights have been obtained by contrasting activity induced by stimulating one neuron (or set of neurons) to activity induced by stimulating a different neuron (or set of neurons). The focus of our work differs. We study one type of motor program, ingestive feeding in the mollusc Aplysia californica, which can either be triggered when a single projection neuron (CBI-2) is repeatedly stimulated or can be triggered by projection neuron coactivation (e.g., activation of CBI-2 and CBI-3). We ask why this might be an advantageous arrangement. The cellular/molecular mechanisms that configure motor activity are different in the two situations because the released neurotransmitters differ. We focus on an important consequence of this arrangement, the fact that a persistent state can be induced with repeated CBI-2 stimulation that is not necessarily induced by CBI-2/3 coactivation. We show that this difference can have consequences for the ability of the system to switch from one type of activity to another.NEW & NOTEWORTHY We study a type of motor program that can be induced either by stimulating a higher-order projection neuron that induces a persistent state, or by coactivating projection neurons that configure activity but do not produce a state change. We show that when an activity is configured without a state change, it is possible to immediately return to an intermediate state that subsequently can be converted to any type of motor program.


Assuntos
Aplysia , Comportamento Alimentar , Animais , Comportamento Alimentar/fisiologia , Aplysia/fisiologia , Ingestão de Alimentos/fisiologia , Interneurônios/fisiologia , Neurônios Motores/fisiologia , Gânglios dos Invertebrados/fisiologia
5.
J Neurophysiol ; 130(3): 569-584, 2023 09 01.
Artigo em Inglês | MEDLINE | ID: mdl-37529838

RESUMO

Recently, activity has been proposed as a primary feedback mechanism used by continuously bursting neurons to coordinate ion channel mRNA relationships that underlie stable output. However, some neuron types only have intermittent periods of activity and so may require alternative mechanisms that induce and constrain the appropriate ion channel profile in different states of activity. To address this, we used the pyloric dilator (PD; constitutively active) and the lateral gastric (LG; periodically active) neurons of the stomatogastric ganglion (STG) of the crustacean Cancer borealis. We experimentally stimulated descending inputs to the STG to cause release of neuromodulators known to elicit the active state of LG neurons and quantified the mRNA abundances and pairwise relationships of 11 voltage-gated ion channels in active and silent LG neurons. The same stimulus does not significantly alter PD activity. Activation of LG upregulated ion channel mRNAs and lead to a greater number of positively correlated pairwise channel mRNA relationships. Conversely, this stimulus did not induce major changes in ion channel mRNA abundances and relationships of PD cells, suggesting their ongoing activity is sufficient to maintain channel mRNA relationships even under changing modulatory conditions. In addition, we found that ion channel mRNA correlations induced by the active state of LG are influenced by a combination of activity- and neuromodulator-dependent feedback mechanisms. Interestingly, some of these same correlations are maintained by distinct mechanisms in PD, suggesting that these motor networks use distinct feedback mechanisms to coordinate the same mRNA relationships across neuron types.NEW & NOTEWORTHY Neurons use various feedback mechanisms to adjust and maintain their output. Here, we demonstrate that different neurons within the same network can use distinct signaling mechanisms to regulate the same ion channel mRNA relationships.


Assuntos
Braquiúros , Neurônios Motores , Animais , Retroalimentação , RNA Mensageiro , Neurônios Motores/fisiologia , Canais Iônicos/genética , Piloro , Gânglios dos Invertebrados/fisiologia , Braquiúros/fisiologia , Rede Nervosa/fisiologia
6.
J Comp Neurol ; 530(17): 2954-2965, 2022 12.
Artigo em Inglês | MEDLINE | ID: mdl-35882035

RESUMO

The crustacean cardiac ganglion (CG) comprises nine neurons that provide rhythmic drive to the heart. The CG is the direct target of multiple modulators. Synapsin-like immunoreactivity was found clustered around the somata of the large cells (LC) and in a neuropil at the anterior branch of the CG trunk of Cancer borealis. This implicates the soma as a key site of synaptic integration, an unusual configuration in invertebrates. Proctolin is an excitatory neuromodulator of the CG, and proctolin-like immunoreactivity exhibited partial overlap with putative chemical synapses near the LCs and at the neuropil. A proctolin-like projection was also found in a pair of excitatory nerves entering the CG. GABA-like immunoreactivity was nearly completely colocalized with chemical synapses near the LCs but absent at the anterior branch neuropil. GABA-like projections were found in a pair of inhibitory nerves entering the CG. C. borealis Allatostatin B1 (CbASTB), red pigment concentrating hormone, and FLRFamide-like immunoreactivity each had a unique pattern of staining and co-localization with putative chemical synapses. These results provide morphological evidence that synaptic input is integrated at LC somata in the CG. Our findings provide a topographical organization for some of the multiple inhibitory and excitatory modulators that alter the rhythmic output of this semi-autonomous motor circuit.


Assuntos
Braquiúros , Neoplasias , Animais , Braquiúros/anatomia & histologia , Gânglios dos Invertebrados/fisiologia , Neurotransmissores , Sinapses , Sinapsinas , Ácido gama-Aminobutírico
7.
eNeuro ; 9(4)2022.
Artigo em Inglês | MEDLINE | ID: mdl-35817566

RESUMO

The levels of voltage-gated and synaptic currents in the same neuron type can vary substantially across individuals. Yet, the phase relationships between neurons in oscillatory circuits are often maintained, even in the face of varying oscillation frequencies. We examined whether synaptic and intrinsic currents are matched to maintain constant activity phases across preparations, using the lateral pyloric (LP) neuron of the stomatogastric ganglion (STG) of the crab, Cancer borealis LP produces stable oscillatory bursts on release from inhibition, with an onset phase that is independent of oscillation frequency. We quantified the parameters that define the shape of the synaptic current inputs across preparations and found no linear correlations with voltage-gated currents. However, several synaptic parameters were correlated with oscillation period and burst onset phase, suggesting they may play a role in phase maintenance. We used dynamic clamp to apply artificial synaptic inputs and found that those synaptic parameters correlated with phase and period were ineffective in influencing burst onset. Instead, parameters that showed the least variability across preparations had the greatest influence. Thus, parameters that influence circuit phasing are constrained across individuals, while those that have little effect simply co-vary with phase and frequency.


Assuntos
Braquiúros , Gânglios dos Invertebrados , Animais , Gânglios , Gânglios dos Invertebrados/fisiologia , Neurônios/fisiologia , Piloro/fisiologia
8.
J Neurophysiol ; 127(6): 1445-1459, 2022 06 01.
Artigo em Inglês | MEDLINE | ID: mdl-35507477

RESUMO

These experiments focus on an interneuron (B63) that is part of the feeding central pattern generator (CPG) in Aplysia californica. Previous work has established that B63 is critical for program initiation regardless of the type of evoked activity. B63 receives input from a number of different elements of the feeding circuit. Program initiation occurs reliably when some are activated, but we show that it does not occur reliably with activation of others. When program initiation is reliable, modulatory neuropeptides are released. For example, previous work has established that an ingestive input to the feeding CPG, cerebral buccal interneuron 2 (CBI-2), releases feeding circuit activating peptide (FCAP) and cerebral peptide 2 (CP-2). Afferents with processes in the esophageal nerve (EN) that trigger egestive motor programs release small cardioactive peptide (SCP). Previous studies have described divergent cellular and molecular effects of FCAP/CP-2 and SCP on the feeding circuit that specify motor activity. Here, we show that FCAP/CP-2 and SCP additionally increase the B63 excitability. Thus, we show that peptides that have well-characterized divergent effects on the feeding circuit additionally act convergently at the level of a single neuron. Since convergent effects of FCAP/CP-2 and SCP are not necessary for specifying the type of network output, we ask why they might be important. Our data suggest that they have an impact during a task switch, i.e., when there is a switch from egestive to ingestive activity.NEW & NOTEWORTHY The activity of multifunctional central pattern generators (CPGs) is often configured by neuromodulators that exert divergent effects that are necessary to specify motor output. We demonstrate that ingestive and egestive inputs to the feeding CPG in Aplysia act convergently (as well as divergently). We ask why this convergence may be important and suggest that it may be a mechanism for a type of arousal that occurs during task switching.


Assuntos
Geradores de Padrão Central , Neuropeptídeos , Animais , Aplysia/fisiologia , Comportamento Alimentar/fisiologia , Gânglios dos Invertebrados/fisiologia , Interneurônios/fisiologia , Neuropeptídeos/farmacologia
9.
Elife ; 112022 03 18.
Artigo em Inglês | MEDLINE | ID: mdl-35302489

RESUMO

Neural circuits can generate many spike patterns, but only some are functional. The study of how circuits generate and maintain functional dynamics is hindered by a poverty of description of circuit dynamics across functional and dysfunctional states. For example, although the regular oscillation of a central pattern generator is well characterized by its frequency and the phase relationships between its neurons, these metrics are ineffective descriptors of the irregular and aperiodic dynamics that circuits can generate under perturbation or in disease states. By recording the circuit dynamics of the well-studied pyloric circuit in Cancer borealis, we used statistical features of spike times from neurons in the circuit to visualize the spike patterns generated by this circuit under a variety of conditions. This approach captures both the variability of functional rhythms and the diversity of atypical dynamics in a single map. Clusters in the map identify qualitatively different spike patterns hinting at different dynamic states in the circuit. State probability and the statistics of the transitions between states varied with environmental perturbations, removal of descending neuromodulatory inputs, and the addition of exogenous neuromodulators. This analysis reveals strong mechanistically interpretable links between complex changes in the collective behavior of a neural circuit and specific experimental manipulations, and can constrain hypotheses of how circuits generate functional dynamics despite variability in circuit architecture and environmental perturbations.


Assuntos
Braquiúros , Gânglios dos Invertebrados , Animais , Braquiúros/fisiologia , Gânglios dos Invertebrados/fisiologia , Neurônios/fisiologia , Neurotransmissores/fisiologia , Piloro/fisiologia
10.
Elife ; 112022 02 01.
Artigo em Inglês | MEDLINE | ID: mdl-35103594

RESUMO

Reciprocal inhibition is a building block in many sensory and motor circuits. We studied the features that underly robustness in reciprocally inhibitory two neuron circuits. We used the dynamic clamp to create reciprocally inhibitory circuits from pharmacologically isolated neurons of the crab stomatogastric ganglion by injecting artificial graded synaptic (ISyn) and hyperpolarization-activated inward (IH) currents. There is a continuum of mechanisms in circuits that generate antiphase oscillations, with 'release' and 'escape' mechanisms at the extremes, and mixed mode oscillations between these extremes. In release, the active neuron primarily controls the off/on transitions. In escape, the inhibited neuron controls the transitions. We characterized the robustness of escape and release circuits to alterations in circuit parameters, temperature, and neuromodulation. We found that escape circuits rely on tight correlations between synaptic and H conductances to generate bursting but are resilient to temperature increase. Release circuits are robust to variations in synaptic and H conductances but fragile to temperature increase. The modulatory current (IMI) restores oscillations in release circuits but has little effect in escape circuits. Perturbations can alter the balance of escape and release mechanisms and can create mixed mode oscillations. We conclude that the same perturbation can have dramatically different effects depending on the circuits' mechanism of operation that may not be observable from basal circuit activity.


Assuntos
Braquiúros , Neurônios , Animais , Braquiúros/fisiologia , Gânglios , Gânglios dos Invertebrados/fisiologia , Neurônios/fisiologia
11.
Curr Biol ; 32(6): 1439-1445.e3, 2022 03 28.
Artigo em Inglês | MEDLINE | ID: mdl-35148862

RESUMO

In many animals, the daily cycling of light is a key environmental cue, encoded in part by specialized light-sensitive neurons without visual functions. We serendipitously discovered innate light-responsiveness while imaging the extensively studied stomatogastric ganglion (STG) of the crab, Cancer borealis. The STG houses a motor circuit that controls the rhythmic contractions of the foregut, and the system has facilitated deep understanding of circuit function and neuromodulation. We illuminated the crab STG in vitro with different wavelengths and amplitudes of light and found a dose-dependent increase in neuronal activity upon exposure to blue light (λ460-500 nm). The response was elevated in the absence of neuromodulatory inputs to the STG. The pacemaker kernel that drives the network rhythm was responsive to light when synaptically isolated, and light shifted the threshold for slow wave and spike activity in the hyperpolarized direction, accounting for the increased activity patterns. Cryptochromes are evolutionarily conserved blue-light photoreceptors that are involved in circadian behaviors.1 Their activation by light can lead to enhanced neuronal activity.2 We identified cryptochrome sequences in the C. borealis transcriptome as potential mediators of this response and confirmed their expression in pyloric dilator (PD) neurons, which are part of the pacemaker kernel, by single-cell RNA-seq analysis.


Assuntos
Braquiúros , Neoplasias , Animais , Braquiúros/fisiologia , Gânglios , Gânglios dos Invertebrados/metabolismo , Neoplasias/metabolismo , Neurônios/fisiologia , Periodicidade
12.
Biochem Biophys Res Commun ; 598: 9-14, 2022 04 02.
Artigo em Inglês | MEDLINE | ID: mdl-35149434

RESUMO

The identification of novel peptides that regulate reproduction is essential for studying reproductive physiology in bivalves. Therefore, we aimed to identify peptides that affect the reproductive physiology of bivalves. We identified an oocyte maturation-, sperm motility-, and spawning-inducing peptide from the visceral ganglia of the pen shell, Atrina pectinata. The peptide consisted of 26 amino acid residues (GFDSINFPGTIDGFKDYSSNKKERLL). This peptide induced oocyte maturation and sperm motility activation at less than 1 nM upon the treatment of gonad fragments and induced spawning at 1 nmol when injected into mature individuals. Mature eggs and sperms artificially spawned by peptide administration were fertilized, and we confirmed that the development proceeded normally to veliger (D-shape) larvae. These results indicated that GFDSINFPGTIDGFKDYSSNKKERLL stimulated the gonads of pen shells and induced oocyte maturation, sperm motility activation, and spawning.


Assuntos
Bivalves/química , Bivalves/fisiologia , Oócitos/efeitos dos fármacos , Peptídeos/farmacologia , Motilidade dos Espermatozoides/efeitos dos fármacos , Animais , Bivalves/efeitos dos fármacos , Clonagem Molecular , Feminino , Gânglios dos Invertebrados/química , Masculino , Oócitos/fisiologia , Ovário/efeitos dos fármacos , Peptídeos/química , Peptídeos/genética , Reprodução/efeitos dos fármacos , Reprodução/fisiologia , Espectrometria de Massas em Tandem , Testículo/efeitos dos fármacos
13.
J Neurophysiol ; 126(6): 1875-1890, 2021 12 01.
Artigo em Inglês | MEDLINE | ID: mdl-34705575

RESUMO

Nervous systems face a torrent of sensory inputs, including proprioceptive feedback. Signal integration depends on spatially and temporally coinciding signals. It is unclear how relative time delays affect multimodal signal integration from spatially distant sense organs. We measured transmission times and latencies along all processing stages of sensorimotor pathways in the stick insect leg muscle control system, using intra- and extracellular recordings. Transmission times of signals from load-sensing tibial and trochanterofemoral campaniform sensilla (tiCS, tr/fCS) to the premotor network were longer than from the movement-sensing femoral chordotonal organ (fCO). We characterized connectivity patterns from tiCS, tr/fCS, and fCO afferents to identified premotor nonspiking interneurons (NSIs) and motor neurons (MNs) by distinguishing short- and long-latency responses to sensory stimuli. Functional NSI connectivity depended on sensory context. The timeline of multisensory integration in the NSI network showed an early phase of movement signal processing and a delayed phase of load signal integration. The temporal delay of load signals relative to movement feedback persisted into MN activity and muscle force development. We demonstrate differential delays in the processing of two distinct sensory modalities generated by the sensorimotor network and affecting motor output. The reported temporal differences in sensory processing and signal integration improve our understanding of sensory network computation and function in motor control.NEW & NOTEWORTHY Networks integrating multisensory input face the challenge of not only spatial but also temporal integration. In the local network controlling insect leg movements, proprioceptive signal delays differ between sensory modalities. Specifically, signal transmission times to and neuronal connectivity within the sensorimotor network lead to delayed information about leg loading relative to movement signals. Temporal delays persist up to the level of the motor output, demonstrating its relevance for motor control.


Assuntos
Gânglios dos Invertebrados/fisiologia , Interneurônios/fisiologia , Extremidade Inferior/fisiologia , Atividade Motora/fisiologia , Neurônios Motores/fisiologia , Rede Nervosa/fisiologia , Propriocepção/fisiologia , Animais , Comportamento Animal/fisiologia , Fenômenos Eletrofisiológicos/fisiologia , Feminino , Insetos
14.
J Neurophysiol ; 126(6): 1903-1924, 2021 12 01.
Artigo em Inglês | MEDLINE | ID: mdl-34669505

RESUMO

Studies elucidating modulation of microcircuit activity in isolated nervous systems have revealed numerous insights regarding neural circuit flexibility, but this approach limits the link between experimental results and behavioral context. To bridge this gap, we studied feeding behavior-linked modulation of microcircuit activity in the isolated stomatogastric nervous system (STNS) of male Cancer borealis crabs. Specifically, we removed hemolymph from a crab that was unfed for ≥24 h ("unfed" hemolymph) or fed 15 min to 2 h before hemolymph removal ("fed" hemolymph). After feeding, the first significant foregut emptying occurred >1 h later and complete emptying required ≥6 h. We applied the unfed or fed hemolymph to the stomatogastric ganglion (STG) in an isolated STNS preparation from a separate, unfed crab to determine its influence on the VCN (ventral cardiac neuron)-triggered gastric mill (chewing) and pyloric (filtering of chewed food) rhythms. Unfed hemolymph had little influence on these rhythms, but fed hemolymph from each examined time-point (15 min, 1 h, or 2 h after feeding) slowed one or both rhythms without weakening circuit neuron activity. There were also distinct parameter changes associated with each time-point. One change unique to the 1-h time-point (i.e., reduced activity of one circuit neuron during the transition from the gastric mill retraction to protraction phase) suggested that the fed hemolymph also enhanced the influence of a projection neuron that innervates the STG from a ganglion isolated from the applied hemolymph. Hemolymph thus provides a feeding state-dependent modulation of the two feeding-related motor patterns in the C. borealis STG.NEW & NOTEWORTHY Little is known about behavior-linked modulation of microcircuit activity. We show that the VCN-triggered gastric mill (chewing) and pyloric (food filtering) rhythms in the isolated crab Cancer borealis stomatogastric nervous system were changed by applying hemolymph from recently fed but not unfed crabs. This included some distinct parameter changes during each examined post-fed hemolymph time-point. These results suggest the presence of feeding-related changes in circulating hormones that regulate consummatory microcircuit activity.


Assuntos
Geradores de Padrão Central/fisiologia , Fenômenos Fisiológicos do Sistema Digestório , Moela não Aviária/fisiologia , Hemolinfa/fisiologia , Periodicidade , Animais , Comportamento Animal , Braquiúros , Comportamento Alimentar , Gânglios dos Invertebrados , Masculino
15.
eNeuro ; 8(6)2021.
Artigo em Inglês | MEDLINE | ID: mdl-34593519

RESUMO

In oscillatory circuits, some actions of neuromodulators depend on the oscillation frequency. However, the mechanisms are poorly understood. We explored this problem by characterizing neuromodulation of the lateral pyloric (LP) neuron of the crab stomatogastric ganglion (STG). Many peptide modulators, including proctolin, activate the same ionic current (IMI) in STG neurons. Because IMI is fast and non-inactivating, its peak level does not depend on the temporal properties of neuronal activity. We found, however, that the amplitude and peak time of the proctolin-activated current in LP is frequency dependent. Because frequency affects the rate of voltage change, we measured these currents with voltage ramps of different slopes and found that proctolin activated two kinetically distinct ionic currents: the known IMI, whose amplitude is independent of ramp slope or direction, and an inactivating current (IMI-T), which was only activated by positive ramps and whose amplitude increased with increasing ramp slope. Using a conductance-based model we found that IMI and IMI-T make distinct contributions to the bursting activity, with IMI increasing the excitability, and IMI-T regulating the burst onset by modifying the postinhibitory rebound in a frequency-dependent manner. The voltage dependence and partial calcium permeability of IMI-T is similar to other characterized neuromodulator-activated currents in this system, suggesting that these are isoforms of the same channel. Our computational model suggests that calcium permeability may allow this current to also activate the large calcium-dependent potassium current in LP, providing an additional mechanism to regulate burst termination. These results demonstrate a mechanism for frequency-dependent actions of neuromodulators.


Assuntos
Braquiúros , Neurotransmissores , Potenciais de Ação , Animais , Gânglios , Gânglios dos Invertebrados , Neurônios , Neurotransmissores/farmacologia , Piloro
16.
Curr Biol ; 31(21): 4831-4838.e4, 2021 11 08.
Artigo em Inglês | MEDLINE | ID: mdl-34506730

RESUMO

A fundamental question in neuroscience is whether neuronal circuits with variable circuit parameters that produce similar outputs respond comparably to equivalent perturbations.1-4 Work on the pyloric rhythm of the crustacean stomatogastric ganglion (STG) showed that highly variable sets of intrinsic and synaptic conductances can generate similar circuit activity patterns.5-9 Importantly, in response to physiologically relevant perturbations, these disparate circuit solutions can respond robustly and reliably,10-12 but when exposed to extreme perturbations the underlying circuit parameter differences produce diverse patterns of disrupted activity.7,12,13 In this example, the pyloric circuit is unchanged; only the conductance values vary. In contrast, the gastric mill rhythm in the STG can be generated by distinct circuits when activated by different modulatory neurons and/or neuropeptides.14-21 Generally, these distinct circuits produce different gastric mill rhythms. However, the rhythms driven by stimulating modulatory commissural neuron 1 (MCN1) and bath-applying CabPK (Cancer borealis pyrokinin) peptide generate comparable output patterns, despite having distinct circuits that use separate cellular and synaptic mechanisms.22-25 Here, we use these two gastric mill circuits to determine whether such circuits respond comparably when challenged with persisting (hormonal: CCAP) or acute (sensory: GPR neuron) metabotropic influences. Surprisingly, the hormone-mediated action separates these two rhythms despite activating the same ionic current in the same circuit neuron during both rhythms, whereas the sensory neuron evokes comparable responses despite acting via different synapses during each rhythm. These results highlight the need for caution when inferring the circuit response to a perturbation when that circuit is not well defined physiologically.


Assuntos
Braquiúros , Gânglios dos Invertebrados , Potenciais de Ação/fisiologia , Animais , Gânglios dos Invertebrados/fisiologia , Rede Nervosa/fisiologia , Neurônios/fisiologia , Periodicidade , Sinapses/fisiologia
17.
Development ; 148(19)2021 10 01.
Artigo em Inglês | MEDLINE | ID: mdl-34415334

RESUMO

Gene regulatory mechanisms that specify subtype identity of central complex (CX) neurons are the subject of intense investigation. The CX is a compartment within the brain common to all insect species and functions as a 'command center' that directs motor actions. It is made up of several thousand neurons, with more than 60 morphologically distinct identities. Accordingly, transcriptional programs must effect the specification of at least as many neuronal subtypes. We demonstrate a role for the transcription factor Shaking hands (Skh) in the specification of embryonic CX neurons in Tribolium. The developmental dynamics of skh expression are characteristic of terminal selectors of subtype identity. In the embryonic brain, skh expression is restricted to a subset of neurons, many of which survive to adulthood and contribute to the mature CX. skh expression is maintained throughout the lifetime in at least some CX neurons. skh knockdown results in axon outgrowth defects, thus preventing the formation of an embryonic CX primordium. The previously unstudied Drosophila skh shows a similar embryonic expression pattern, suggesting that subtype specification of CX neurons may be conserved.


Assuntos
Axônios/metabolismo , Proteínas de Homeodomínio/metabolismo , Proteínas de Insetos/metabolismo , Crescimento Neuronal , Fatores de Transcrição/metabolismo , Tribolium/metabolismo , Animais , Axônios/fisiologia , Gânglios dos Invertebrados/citologia , Gânglios dos Invertebrados/metabolismo , Proteínas de Homeodomínio/química , Proteínas de Homeodomínio/genética , Proteínas de Insetos/química , Proteínas de Insetos/genética , Domínios Proteicos , Fatores de Transcrição/química , Fatores de Transcrição/genética , Tribolium/embriologia , Tribolium/genética
18.
J Neurosci ; 41(37): 7848-7863, 2021 09 15.
Artigo em Inglês | MEDLINE | ID: mdl-34349000

RESUMO

Oscillatory networks underlie rhythmic behaviors (e.g., walking, chewing) and complex behaviors (e.g., memory formation, decision-making). Flexibility of oscillatory networks includes neurons switching between single- and dual-network participation, even generating oscillations at two distinct frequencies. Modulation of synaptic strength can underlie this neuronal switching. Here we ask whether switching into dual-frequency oscillations can also result from modulation of intrinsic neuronal properties. The isolated stomatogastric nervous system of male Cancer borealis crabs contains two well-characterized rhythmic feeding-related networks (pyloric, ∼1 Hz; gastric mill, ∼0.1 Hz). The identified modulatory projection neuron MCN5 causes the pyloric-only lateral posterior gastric (LPG) neuron to switch to dual pyloric/gastric mill bursting. Bath applying the MCN5 neuropeptide transmitter Gly1-SIFamide only partly mimics the LPG switch to dual activity because of continued LP neuron inhibition of LPG. Here, we find that MCN5 uses a cotransmitter, glutamate, to inhibit LP, unlike Gly1-SIFamide excitation of LP. Thus, we modeled the MCN5-elicited LPG switching with Gly1-SIFamide application and LP photoinactivation. Using hyperpolarization of pyloric pacemaker neurons and gastric mill network neurons, we found that LPG pyloric-timed oscillations require rhythmic electrical synaptic input. However, LPG gastric mill-timed oscillations do not require any pyloric/gastric mill synaptic input and are voltage-dependent. Thus, we identify modulation of intrinsic properties as an additional mechanism for switching a neuron into dual-frequency activity. Instead of synaptic modulation switching a neuron into a second network as a passive follower, modulation of intrinsic properties could enable a switching neuron to become an active contributor to rhythm generation in the second network.SIGNIFICANCE STATEMENT Neuromodulation of oscillatory networks can enable network neurons to switch from single- to dual-network participation, even when two networks oscillate at distinct frequencies. We used small, well-characterized networks to determine whether modulation of synaptic strength, an identified mechanism for switching, is necessary for dual-network recruitment. We demonstrate that rhythmic electrical synaptic input is required for continued linkage with a "home" network, whereas modulation of intrinsic properties enables a neuron to generate oscillations at a second frequency. Neuromodulator-induced switches in neuronal participation between networks occur in motor, cognitive, and sensory networks. Our study highlights the importance of considering intrinsic properties as a pivotal target for enabling parallel participation of a neuron in two oscillatory networks.


Assuntos
Potenciais de Ação/fisiologia , Geradores de Padrão Central/fisiologia , Rede Nervosa/fisiologia , Neurônios/fisiologia , Animais , Braquiúros , Gânglios dos Invertebrados/fisiologia
19.
Cell ; 184(18): 4819-4837.e22, 2021 09 02.
Artigo em Inglês | MEDLINE | ID: mdl-34380046

RESUMO

Animal bodies are composed of cell types with unique expression programs that implement their distinct locations, shapes, structures, and functions. Based on these properties, cell types assemble into specific tissues and organs. To systematically explore the link between cell-type-specific gene expression and morphology, we registered an expression atlas to a whole-body electron microscopy volume of the nereid Platynereis dumerilii. Automated segmentation of cells and nuclei identifies major cell classes and establishes a link between gene activation, chromatin topography, and nuclear size. Clustering of segmented cells according to gene expression reveals spatially coherent tissues. In the brain, genetically defined groups of neurons match ganglionic nuclei with coherent projections. Besides interneurons, we uncover sensory-neurosecretory cells in the nereid mushroom bodies, which thus qualify as sensory organs. They furthermore resemble the vertebrate telencephalon by molecular anatomy. We provide an integrated browser as a Fiji plugin for remote exploration of all available multimodal datasets.


Assuntos
Forma Celular , Regulação da Expressão Gênica , Poliquetos/citologia , Poliquetos/genética , Análise de Célula Única , Animais , Núcleo Celular/metabolismo , Gânglios dos Invertebrados/metabolismo , Perfilação da Expressão Gênica , Família Multigênica , Imagem Multimodal , Corpos Pedunculados/metabolismo , Poliquetos/ultraestrutura
20.
Peptides ; 144: 170610, 2021 10.
Artigo em Inglês | MEDLINE | ID: mdl-34242680

RESUMO

Only few genes are known from insects that encode multiple neuropeptides, i.e., peptides that activate different receptors. Among those are the capa and pk genes, which differentiated within Hexapoda following gene duplication. In our study, we focus on the early stages of differentiation of these genes. Specifically: (1) What was the expression pattern of the ancestral capa/pk gene, i.e., prior to gene duplication? (2) What is the expression pattern of capa and pk in silverfish, whose ancestors diverged from Pterygota more than 400 mya? Our results suggest the location and projection of CAPA immunoreactive Va cells in abdominal ganglia (trunk ganglia in Remipedia) are a plesiomorphic trait that was already present in the ancestor of Remipedia and Hexapoda. General features of serial homology such as location of cells bodies, contralateral projection of primary neurites, and presumed peripheral peptide release from segmentally arranged neurohemal release sites could be observed in Remipedia and silverfish, but also in all Pterygota studied so far. Differences are mainly in the specific location of these peripheral release sites. This hypothetical basic pattern of capa/pk neurons underwent modifications in the anterior ganglia of the ventral nerve cord already in Remipedia. In silverfish, as in all Pterygota studied so far, pk expression in the CNS is apparently restricted to the gnathal ganglia, whereas capa expression is typical of abdominal Va cells. Thus, differentiation in the expression pattern of capa and pk genes occurred early in the evolution of Hexapoda; likely soon after the appearance of two separate genes.


Assuntos
Crustáceos/genética , Proteínas de Peixes/genética , Lepisma/genética , Neuropeptídeos/genética , Animais , Evolução Molecular , Proteínas de Peixes/metabolismo , Gânglios dos Invertebrados/fisiologia , Duplicação Gênica , Expressão Gênica , Proteínas de Insetos/genética , Neuropeptídeos/metabolismo , Espectrometria de Massas por Ionização e Dessorção a Laser Assistida por Matriz
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