{R}egulation of motor patterns by the central spike-initiation zone of a sensory neuron (original) (raw)
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Neuronal release of modulatory substances provides motor pattern generating circuits with a high degree of flexibility. In vitro studies have characterized the actions of modulatory projection neurons in great detail in the stomatogastric nervous system, a model system for neuromodulatory influences on central pattern generators. Less is known about the activities and actions of modulatory neurons in fully functional and richly modulated network settings, i.e., in intact animals. It is also unknown whether their activities contribute to the motor patterns in different behavioral conditions. Here, we show for the first time the activity and effects of the well-characterized modulatory projection neuron 1 (MCN1) in vivo and compare them to in vitro conditions. MCN1 was always spontaneously active, typically in a rhythmic fashion with its firing being interrupted by ascending inhibitions from the pyloric motor circuit. Its activity contributed to pyloric motor activity, because 1) the cycle period of the motor pattern correlated with MCN1 firing frequency and 2) stimulating MCN1 shortened the cycle period while 3) lesioning of the MCN1 axon reduced motor activity. In addition, gastric mill motor activity was elicited for the duration of the stimulation. Chemosensory stimulation of the antennae moved MCN1 away from baseline activity by increasing its firing frequency. Following this increase, a gastric mill rhythm was elicited and the pyloric cycle period decreased. Lesioning the MCN1 axon prevented these effects. Thus modulatory projection neurons such as MCN1 can control the motor output in vivo, and they participate in the processing of exteroceptive sensory information in behaviorally relevant conditions.
Co-transmission is a common means of neuronal communication, but its consequences for neuronal signaling within a defined neuronal circuit remain unknown in most systems. We are addressing this issue in the crab stomatogastric nervous system by characterizing how the identified modulatory commissural neuron (MCN)1 uses its co-transmitters to activate the gastric mill (chewing) rhythm in the stomatogastric ganglion (STG). MCN1 contains gamma-aminobutyric acid (GABA) plus the peptides proctolin and Cancer borealis tachykinin-related peptide Ia (CabTRP Ia), which it co-releases during the retractor phase of the gastric mill rhythm to influence both retractor and protractor neurons. By focally applying each MCN1 co-transmitter and pharmacologically manipulating each co-transmitter action during MCN1 stimulation, we found that MCN1 has divergent co-transmitter actions on the gastric mill central pattern generator (CPG), which includes the neurons lateral gastric (LG) and interneuron 1 (Int1), plus the STG terminals of MCN1 (MCN1(STG)). MCN1 used only CabTRP Ia to influence LG, while it used only GABA to influence Int1 and the contralateral MCN1(STG). These MCN1 actions caused a slow excitation of LG, a fast excitation of Int1 and a fast inhibition of MCN1(STG). MCN1-released proctolin had no direct influence on the gastric mill CPG, although it likely indirectly regulates this CPG via its influence on the pyloric rhythm. MCN1 appeared to have no ionotropic actions on the gastric mill follower motor neurons, but it did use proctolin and/or CabTRP Ia to excite them. Thus, a modulatory projection neuron can elicit rhythmic motor activity by using distinct co-transmitters, with different time courses of action, to simultaneously influence different CPG neurons.
Sensorimotor integration is known to occur at the level of motor circuits as well as in upstream interneurons that regulate motor activity. Here we show, using the crab stomatogastric nervous system (STNS) as a model, that different sensory systems affect the same set of projection neurons. However, they have qualitatively different effects on their activities (excitation vs. inhibition), and these differences contribute to the selection of motor patterns from multifunctional circuits. We compare the actions of the proprioceptive anterior gastric receptor (AGR) and the inferior ventricular (IV) neurons, which relay chemosensory information from the brain to the STNS, on modulatory commissural neurons 1 and 5 (MCN1 and MCN5) and commissural projection neuron 2 (CPN2) and their resulting actions on the gastric mill central pattern generating circuit in the stomatogastric ganglion. When stimulated, AGR and the IV neurons affect all three projection neurons but elicit distinct gastric mill rhythms. The effects of both sensory pathways on the projection neurons differ in the type of excitation provided to CPN2 and MCN5 (electrical vs. chemical) and the effect on MCN1 (direct inhibition by AGR vs. polysynaptic excitation by the IV neurons). The latter is functionally important because a restoration of MCN1 activity during the AGR rhythm made it more similar to that elicited by IV neuron stimulation. Our results thus support the hypothesis that sensory pathways activate different combinations of projection neurons to select distinct outputs from the same neuronal circuit.
A Cellular Mechanism for the Transformation of a Sensory Input into a Motor Command
2000
The initiation and control of locomotion largely depend on processing of sensory inputs. The cellular bases of locomotion have been extensively studied in lampreys where reticulospinal (RS) neurons constitute the main descending system activating and controlling the spinal locomotor networks. Ca 2ϩ imaging and intracellular recordings were used to study the pattern of activation of RS neurons in response to cutaneous stimulation. Pressure applied to the skin evoked a linear input/output relationship in RS neurons until a threshold level, at which a depolarizing plateau was induced, the occurrence of which was associated with the onset of swimming activity in a semi-intact preparation. The occurrence of a depolarizing plateau was abolished by blocking the NMDA receptors that are located on RS cells.
Basic Principles for Generating Motor Output in the Stomatogastric Ganglion
Annals of the New York Academy of Sciences, 1998
The lobster stomatogastric ganglion contains 30 neurons and when modulated can produce two distinct rhythmic motor patterns-the gastric mill and the pyloric. The complete neural circuitry underlying both patterns is well known. Without modulatory input no patterns are produced, and the neurons fire tonically or are silent. When neuromodulators are released into the ganglion from specific neurons or are delivered as hormones, the properties of the neurons and synapses change dramatically and modulator-specific gastric mill and pyloric patterns are produced. In general the rhythmicity derives from the induced burstiness of the neurons, and the pattern from the strengths of the electrical and chemical synapses. The organized activity can be traced to a marked reduction of chaotic activity in individual neurons when they shift from the unmodulated to the modulated state.
Presynaptic control of modulatory fibers by their neural network targets
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1992
Numerous modulatory fibers control the output of the pyloric and gastric mill neural networks in the crustacean stomatogastric ganglion (STG). We now describe the first results of intracellular recordings from the axon of one of these input neurons, stomatogastric nerve axon 1 (SNAX 1), close to where it enters the STG. SNAX 1 excites both the pyloric and gastric mill rhythms and is identified on the basis of its synaptic interactions with identified STG neurons. SNAX 1 receives synaptic input from several sources within the STG. As a result of these synaptic inputs, SNAX 1 fires bursts of action potentials that are time-locked to both the pyloric and gastric mill rhythms. The synaptic connections made onto the SNAX axon terminals are likely to play important roles in shaping the impulse activity patterns in these modulatory inputs. Thus, the fibers that modulate the pattern-generating networks in the STG are themselves influenced by elements in these networks, and modulation is a d...
PLoS ONE, 2011
After a meal, the gastrointestinal tract exhibits a set of behaviours known as the fed state. A major feature of the fed state is a little understood motor pattern known as segmentation, which is essential for digestion and nutrient absorption. Segmentation manifests as rhythmic local constrictions that do not propagate along the intestine. In guinea-pig jejunum in vitro segmentation constrictions occur in short bursts together with other motor patterns in episodes of activity lasting 40-60 s and separated by quiescent episodes lasting 40-200 s. This activity is induced by luminal nutrients and abolished by blocking activity in the enteric nervous system (ENS). We investigated the enteric circuits that regulate segmentation focusing on a central feature of the ENS: a recurrent excitatory network of intrinsic sensory neurons (ISNs) which are characterized by prolonged after-hyperpolarizing potentials (AHPs) following their action potentials. We first examined the effects of depressing AHPs with blockers of the underlying channels (TRAM-34 and clotrimazole) on motor patterns induced in guinea-pig jejunum, in vitro, by luminal decanoic acid. Contractile episode durations increased markedly, but the frequency and number of constrictions within segmenting bursts and quiescent period durations were unaffected. We used these observations to develop a computational model of activity in ISNs, excitatory and inhibitory motor neurons and the muscle. The model predicted that: i) feedback to ISNs from contractions in the circular muscle is required to produce alternating activity and quiescence with the right durations; ii) transmission from ISNs to excitatory motor neurons is via fast excitatory synaptic potentials (EPSPs) and to inhibitory motor neurons via slow EPSPs. We conclude that two rhythm generators regulate segmentation: one drives contractions within segmentation bursts, the other the occurrence of bursts. The latter depends on AHPs in ISNs and feedback to these neurons from contraction of the circular muscle.
Journal of neurophysiology, 1998
Rhythm generation by the gastric motor network in the stomatogastric ganglion (STG) of the lobster Homarus gammarus is controlled by modulatory projection neurons from rostral commissural ganglia (CoGs); blocking action potential conduction in these inputs to the STG of a stomatogastric nervous system in vitro rapidly renders the gastric network silent. However, exposure of the CoGs to low Ca2+ saline to block chemical synapses activates a spontaneously silent gastric network or enhances an ongoing gastric rhythm. A similar permissive effect was observed when picrotoxin was also superfused on these ganglia. We conclude that in the CoGs continuous synaptic inhibition is exerted on modulatory projection neuron(s) and that release from this inhibition allows strong activation of the gastric network.
Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1999
We have explored the synaptic and cellular mechanisms by which a single primary mechanosensory neuron, the anterior gastric receptor (AGR), reconfigures motor output of the gastric mill central pattern generator (CPG) in the stomatogastric nervous system (STNS) of the lobster Homarus gammarus. AGR is activated in vivo by contraction of the medial tooth protractor muscle gm1 and accesses the gastric CPG via excitation of two in-parallel interneurons, the excitatory commissural gastric (CG) and the inhibitory gastric inhibitor (GI). In the spontaneously active STNS in vitro, weak firing of AGR in time with gastric mill motoneurons (GM) reinforces an ongoing type I gastric mill rhythm in which all gastric teeth power-stroke motoneurons are synchronously active. With strong AGR firing, these phase relationships switch abruptly to a type II pattern in which lateral and medial teeth power-stroke motoneurons fire in antiphase. Our results suggest that these bimodal actions on the gastric m...
Sensory-induced modification of two motor patterns in the crab, Cancer pagurus
Journal of Experimental Biology, 2007
SUMMARYSensory input is pervasive among motor networks and continuously adapts motor patterns to changing circumstances. To elucidate common principles of sensorimotor integration, it is beneficial to characterize sensory influences on motor network operation and compare these influences between species. To facilitate such comparison, we have studied the influence of the anterior gastric receptor (AGR) – a proprioceptor that has been characterized in detail in two lobster species – on the pyloric (filtering of food) and gastric mill (chewing of food) motor patterns in the crab Cancer pagurus.AGR has a bipolar cell body in the stomatogastric ganglion; it was activated by tension increase in gastric mill powerstroke muscles. While two spike initiation zones accounted for its spontaneous activity, active membrane properties (sag potentials, spike frequency adaptation) contributed to the AGR response to current injections.When activated, AGR diminished spike activities in two pyloric mo...