Overview of the Stomatogastric Nervous System


  • Stomatogastric Ganglion

    a. Activity patterns: The stomatogastric ganglion (STG) of crustaceans controls and coordinates the activity of around 40 pairs of striated muscles of the stomach. It possesses around 30 reidentifiable neurons [F2] which are mostly motorneurons. These produce two primary activity rhythms of motor output. The pyloric rhythm causes coordinated sequences of contraction in muscles controlling the pylorus (operating hair-plates). The gastric rhythm controls muscles of the gastric mill (operating the gastric teeth). The ganglion can be excised from the animal along with its sensory, motor, and central nerve connections and kept alive in a Petri dish under physiological saline. Fine wires placed in contact with the nerves and insulated from the saline with vaseline pick up electrical nerve impulse signals travelling out the nerves to the severed muscle connections. Axons to different muscles discharge bursts of impulses which correspond well to the EMG patterns in more intact preparations. The pyloric pattern is characterized by a three-part cycle, in which a burst of impulses in the network driver neurons (PD/AB) is followed by a burst in the motorneuron to the antagonist muscle (LP) and finally a barrage of impulses to more posterior muscles controlling pyloric sieve plates (PE/PL). The gastric pattern consists of alternating bursts in two semi-independent antagonistically arranged motor groups, one controlling the lateral teeth and one controlling the medial tooth.

    b. Synaptic connections: The different motor patterns observed can be explained partly by the synaptic connections and properties among stomatogastric neurons and partly by intrinsic properties of the neurons themselves. Both chemical and electrical connections are found. Most chemical connections within the ganglion ("intrinsic" connections) are inhibitory. In the pyloric system the driver neurons (PD/AB) put strong inhibitory synapses on the remaining "follower" neurons so that during driver activity, followers are shut off. After driver bursts terminate spontaneously, followers are free to fire in a sequence which is determined partly by their synaptic connections and partly by their cellular properties. In the gastric system, antagonistic neurons of the lateral tooth set are reciprocally inhibitorily interconnected, while the driver neurons of the medial tooth (return stroke) inhibit their antagonists, but not the reverse. The synaptic wiring of the gastric system is substantially more complex than that of the pyloric.

    c. Cellular properties: In addition to fairly conventional repetitive firing properties, stomatogastric neurons possess three special cellular properties which significantly shape their activity patterns. A delaying mechanism is activated in some cells upon release from a hyperpolarization, and retards the recovery of the cell from previous synaptic inhibition. A post-inhibitory rebound [F11] mechanism is activated in some cells upon release from a hyperpolarization and promotes rapid recovery and vigorous firing following release from previous synaptic inhibition. A plateau mechanism [F12] endows many cells with an endogenous burst-promoting property which can lead to endogenous repetitive bursting in some cases (in driver cells) or regenerative burst triggering and suppression in others.

    Additional information: calcium currents

    d. Central control: The ganglion is under the control of higher centers. Almost all bursting activity ceases when input from these centers is blocked. The activity can be restored by stimulating input nerves [F13] electrically. The key mechanism by which this control is exerted is through the modulatory regulation of the plateau mechanism. Induction of plateau properties [F14] in specific STG target neurons can occur when specific inputs are stimulated, or when they are exposed to specific neuromodulator substances (presumably) contained in those input neurons. Modulatory control of synaptic strength is also found in the system.

    e. Cellular morphology: Motorneurons of the stomatogastric ganglion are monopolar cells with a cell body located on the outer surface of the ganglion, a main neurite traveling through the neuropile in a typically contorted path and finally exiting as an axon projecting to target muscle(s). For a distance of a few hundred microns along the main neurite, secondary neurites are given off which branch repeatedly into the ganglionic neuropile. The soma is "inexcitable" as far as impulses are concerned, but it shows strong rectification and in some cells exhibits a delaying mechanism. Nerve impulses appear to be confined to the axons. Synaptic inputs and outputs occur on the finer distal branches of the cell, and plateau properties are assumed to reside close to synaptic input sites (given their dependence on modulatory inputs).

    Additional information: Hartline-Graubard-Wilensky 2005 (unpublished manuscript)

    f. Synaptic properties: Electrotonic synapses [F15] tend to occur between synergistic neurons, but this is not universally the case. Rectifying electrotonic connections are common, and modulation of the strength of electrotonic connections by neuromodulators has been reported. Chemical synapses are of two types, spike mediated (phasic) and tonic. Glutamatergic chemical synapses produce rapidly-rising IPSPs in target neurons, while cholinergic IPSPs are much slower to rise. The difference may promote phase shifts and different roles for otherwise similar presynaptic neurons. Chemotonic interactions [F17] probably employ the same release sites and mechanisms as do phasic PSPs, but they are activated by slow membrane voltage changes and do not require spiking in presynaptic neurons. They are quite strong and can coordinate the modulator-induced oscillations of the STG in the presence of tetrodotoxin (TTX), which eliminates all spikes.

    g. Neurotransmitters and neuromodulators: A large number of substances is found with neuromodulatory action on typically very specific groups of cells within the stomatogastric nervous system. The neuromodulators undoubtedly act via one or more of the conventianal second messenger systems, but to date studies on this have been limited.

    Additional information: cAMP studies, cGMP studies.

    h. Modeling.

    i. Pyloric network

    j. Gastric network


    a. Coupled networks

    b. Sensory components

    c. Anatomy

    d. Behavior

    e. Neuromuscular physiology

    f. Comparative and evolutionary aspects


    Anatomy of the spiny lobster stomach


    The figure below shows a diagram of the stomach of a spiny lobster (Panulirus) with muscles color coded according to phase of contraction in the motor patterns (labels with lower case letters and numbers), nerves (heavy black lines) and ganglia of the stomatogastric nervous system (STG = stomatogastric ganglion; OG=oesophageal ganglion; CG=commissural ganglion).

    (source: Hartline and Maynard 1975 Fig. 1)

    Pyloric pattern


    The "pyloric" pattern of motor activity in the intact spiny lobster (Panulirus involves a three-part cycle as shown in the electromyogram (EMG) recordings below. This activity controls a set of sieve plates and valves in the posterior region of the stomach. It apparently sieves food particles and may mix them with digestive secretions.

    (source: Hartline and Maynard 1975 Fig. 5A)

    Pyloric muscle sequence


    The muscles active at each phase of the pyloric cycle are shown in the diagram below. Activity of the pyloric dilator muscles mediated by the two PD neurons appears to open a valve to the pyloric region which is then closed in the second phase by an antagonist, the lateral pyloric muscle operated by the LP cell. In the third phase, a sheet of pyloric muscles contracts under the activation of several PY neurons (divisible into PE and PL subtypes) giving overall a peristaltic appearance to the pyloric surface. The two muscles located on the anterior (cardiac) portion of the stomach control a curious valve structure, the operation of which is described in Squilla (ref: Tazaki)

    (source: Hartline and Maynard, 1975 Fig 4)

    Gastric pattern


    The gastric motor pattern involves two coupled muscle-contraction sequences that operate the gastric mill. EMGs from these muscles are shown in the figure below. Alternation between closer and opener muscles for the lateral teeth is controlled by the LC/GP - LG motorneurons [also called LG/MG - LPG] *. Alternation between protractor and retractor muscles for the medial tooth is controlled by GM - CP [also called DG] *.

    (source: Hartline and Maynard, 1975Fig.3A)

    Gastric mill muscle sequence


    Loose coupling between the two tooth groups generates a coordinated pattern such that GM firing commences usually somewhat after the LC/GP * firing. Thus the power stroke (closer activity) of the lateral teeth occurs somewhat before that of the medial tooth (protraction), and the reverse sequence of return stroke muscle activity is similarly phase shifted, as shown in the diagram below.

    (Source: Hartline and Maynard, 1975, Fig.4)

    Gastric mill operation


    The diagram below shows the two sets of gastric mill teeth, the lateral teeth (top) and the medial tooth (below) along with the primary muscles operating them. The contraction sequence described above and indicated by bars below the tooth diagrams apparently clamps food in the lateral teeth, whereupon the medial tooth rasps down and forward over the immobilized food, helping to macerate it.

    (Source: Hartline and Maynard, 1975, Fig.2)

    Stomatogastric nervous system in a dish


    The diagram below shows the various input and output nerves to the stomatogastric ganglion (STG) as seen in a typical "combined" preparation (see Russell 1976). Nerves going to single muscles or small groups of muscles may be individually followed, freed, and recorded from. The left and right commissural ganglia (CG) can be removed along with segments of the paired circumoesophageal commissures. From these ganglia, two nerves, the inferior (Ion) and superior (Son) oesophageal nerves diverge and then reconverge at the oesophageal ganglion (OG), forming the stomatogastric nerve (Stn), the primary input to the STG. Specific reidentifiable input axons run in these different nerves.

    Nerve impulse discharge patterns from pyloric neurons


    The same coordinated patterns of pyloric activity can be recorded in excised ganglia from electrodes placed on the motor nerves traveling from the ganglion to the muscle. In this recording, connections to the CNS have been left intact and the ganglion is cycling spontaneously. The pattern consists of sequential bursts in three driver neurons (2 PD motorneurons and one AB interneuron), then LP and IC, and finally PE and PL (=PY). The VD burst typically precedes PD/AB and may overlap it.

    (source: Hartline et al.1988, Fig.6)

    See Scott Hooper's web page for an update on recent studies of phase maintenance and pattern generation in the pyloric network.

    Nerve impulse patterns from gastric neurons


    In the absence of connections to the CNS, the gastric motor pattern is completely absent. In the recording below, a "command" fiber" in the input nerve (stomatogastric nerve) is being stimulated at low frequency (ca 2 Hz), which restores active cycling to the gastric network.

    (Source: Russell and Hartline, 1984, Fig.2)

    Pyloric circuit wiring

    (simplified; Panulirus)

    Intracellular recordings from pyloric somata reveal a variety of subthreshold events. Particularly evident are inhibitory synaptic potentials which can be matched 1:1 with identified inpulses in other cells. This serves to establish a "wiring diagram" for the system. The PD/AB cells normally dominate the network through their strong inhibitory synapses onto all other pyloric neurons. When the endogenously-generated PD/AB burst terminates, the other "follower" neurons fire in sequence. In spiny lobsters (Panulirus), LP activity inhibits PD/AB and also weakly inhibits the PYs. PL activity strongly inhibits the LP. Both AB and LP strongly inhibit the VD. In addition, there are bidirectional electrotonic connections in the PD-AB-VD group and among PLs, and a rectifying connection from LP to PLs.

    (Source: Russell and Hartline, 1982, Fig.2)

    Gastric circuit wiring

    (Panulirus; simplified)
    Connections among gastric neurons can be determined through intracellular recordings as they are for the pyloric system. The reciprocal inhibition between the antagonistic groups of lateral teeth motorneurons (LC/GP [LG/MG] and LG [LPG] ensures little overlap in activation of members of the pair. The inhibition from AM/CP[DG] onto GM helps keep separate the activity of those two antagonistic groups. The other connections are complex and how they relate to observed activity is not clear. It was originally thought that no properties capable of producing endogenous bursting are present in the gastric net, so that gastric bursting is an "emergent property" of the synaptic connectivity. Now it is recognized that a complex of cellular and synaptic properties, including in some cases endogenous bursting, are responsible for gastric patterns.

    (Source: Hartline et al.,1988, Fig.1D)

    Repetitive firing properties

    One reason for the focus of so many research efforts on the stomatogastric ganglion is that it has so few cells. There is hope that each cell and each intercellular interaction can be characterized and its contribution to the network activity accurately assessed. To make such an assessment, quantitative measurements must be made of all such properties. The figure below shows how repetitive firing characteristics of STG neruons may be measured by fairly conventional means. Firing in response to a step depolarization is measured as a function of time after current onset. The frequency adapts along a compound exponential timne-course with time-constants that are independent of the strength of the injected current. The numerical values of parameters characterizing this response can be utilized in quantitatively accurate computer models to predict the firing behavior under a variety of other conditions, including natural ocillations.

    (Source: Hartline and Graubard, 1992, Fig.2.13)

    Delaying properties

    Some stomatogastric neurons show a pronounced delay in recovery of their excitability following a brief hyperpolarization, whether synaptically or artificially generated. In the figure below, two different pyloric follower cells are given equal step excitations (top trace of each panel) producing the same rate of impulse firing. If the step excitation is preceded by a hyperpolarizing pre-pulse, there is a delay in the onset of firing while the cell recovers from the hyperpolarization. As the hyperpolarization is increased in magnitude (successive sweeps below the control), the delay in the PY cell becomes disproportionately long compared to that in the LP. A slowly inactivating "A" conductance appears to underlie this phenomonen. It contributes to the phase lag of PY firing relative to LP in the pyloric cycle.

    (Source: Hartline, 1979, Fig. 7)

    See Scott Hooper's web page for an update on recent studies of rebound delay in the pyloric network.

    Postinhibitory rebound


    Certain STG neurons (the LP in the panels below) exhibit a "sag" trajectory when a sufficiently strong hyperpolarizing current (or synaptic inhibition) is injected (left panel). The resulting depolarization brings the neuron closer to threshold despite the maintenance of the suppressing influence. Once the hyperpolarizing input is released, the cell reaches threshold rapidly, and its firing is augmented in a rebound effect that enhances temporal contrast in its activity and adds to the strength of its synaptic output. One paradoxical effect of this mechanism, shown in the panel to the right, is that the TOTAL number of nerve impulses

    (Source: Hartline and Graubard, 1992, Fig.2.15)

    Plateau properties

    If an actively bursting stomatogastric neuron is held silent by a small hyperpolarizing current, it is frequently possible to elicit complete bursts as all-or-nothing responses to brief depolarizing currents or synaptic inputs. These bursts are underlain by an active depolarizing potential termed a "plateau potential", by analogy to the plateau phase of a heart muscle actin potential. Conditions for triggering plateau potentials include a threshold for intensity of the triggering stimulus which must be exceeded to be successful (upper traces in panel A below). Once triggered, a plateau can be terminated in a all-or-nothing manner by a hyperpolarizing stimulus of sufficient magnitude (panel B below). Plateau potentials are turned on and off, sometimes spontaneously and sometimes by impinging synaptic input, in the normal course of cyclic bursting by the STG. They provide a major component of the drive that generates burst firing, as well as contributing critically to the timing of bursts in the stomatogastric system.

    (Source: Hartline et al. 1988, Fig.2)

    Activation of pyloric rhythm by input stimulation

    In isolated ganglia, both pyloric and gastric activity is at a very low level. The pyloric activity pattern can be reactivated in the isolated ganglion by supplying "priming" stimulation to the input (stomatogastric) nerve, as shown in the figure below.

    (Source: Hartline and Maynard, 1975, Fig.5)

    Plateau induction

    (Source: Hartline et al. 1988, Fig.5)

    Electrotonic interactions

    Direct low-pass electrical coupling exists between several of the pairs of STG neurons. Current injected into one of the members of the pair is reflected as an attenuated voltage perturbation of the same sign in the coupled cell. In many cases in STG, the coupling is bidirectional: injection of current in the second cell results in a voltage perturbation of the first. In a few cases, the connection is "rectifying": current of one sign produces a larger perturbation in the postjunctional cell than current of the opposite sign. In such cases, the relation is reversed for current injected into the second cell. The figure below shows the latter case. Hyperpolarizing current injected into the LP (top trace) produces very little hyperpolarization of the postjunctional PL, whereas the same magnitude of depolarizing current (which also generates a train of closely spaced nerve impulses) produces a larger depolarization of the PL. Hyperpolarizing current injected into the PL (bottom trace) produces a large hyperpolarization of the postjunctional LP. Not only does depolarizing current to the PL have little effect on the LP, but its activation of strong chemical synaptic release from PL causes a net hyperpolarization of the LP.

    (Source: Graubard and Hartline, unpublished)

    Synaptic properties

    The figure below shows samples of IPSPs in the pyloric net for interactions among the three principal pyloric cell types. Note the substantial difference in shape for PD-produced IPSPs as compared those produced by AB. PDs are cholinergic, while AB is glutamatergic (ref: Marder). The numbers beside the synapses in the diagram represent the strengths of the particular synapses measured as the number of impulses a single IPSP is capable of deleting from an on-going train in the postsynaptic cell.

    (source: Hartline and Gassie, 1979)

    Additional information: inhibitory glutamate currents

    Chemotonic properties




    (source: , Fig. )

    (To be continued ...)

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