Quantification of Gastric Mill Network Effects on a Movement Related Parameter of Pyloric Network Output in the Lobster

2002 ◽  
Vol 87 (5) ◽  
pp. 2372-2384 ◽  
Author(s):  
Jeff B. Thuma ◽  
Scott L. Hooper

It has long been known that gastric mill network activity (cycle period 5–10 s) alters pyloric network output (cycle period approximately 1 s), but these effects have not been quantified. Many pyloric muscles extract gastric mill timed variations in pyloric motor neuron firing, and consequently produce gastric mill timed movements even though no gastric mill neurons innervate them. Determining pyloric behavior therefore requires detailed description of gastric mill effects on pyloric neural output. Pyloric muscle activity correlates well with motor neuron overall spike frequency (OSF, burst spike number divided by cycle period). We quantified OSF variation of all pyloric neurons as a function of time into the gastric mill cycle [as measured from the beginning of Gastric Mill (GM) neuron bursts] in the lobster, Panulirus interruptus. No repeating pattern within individual gastric mill cycles of Lateral Pyloric (LP) and Ventricular Dilator (VD) neuron OSF was visually apparent. Averaged data showed that VD and LP neuron OSF decreased (approximately 0.5 and 1.5 Hz, respectively) at the beginning of each gastric mill cycle. Visually apparent patterns of OSF waxing and waning within each gastric mill cycle were present for the Inferior Cardiac (IC), Pyloric Dilator (PD), and Pyloric (PY) neurons. However, when averaged as a function of phase or delay in the gastric mill cycle, the average changes were smaller than those in individual gastric mill cycles because when the OSF variations occurred varied considerably in different gastric mill cycles. We therefore used a “pattern-based” analysis in which an identifying characteristic of each neuron's repeating OSF variation pattern was defined as pattern pyloric cycle zero. The pyloric cycles in each repetition of the OSF variation pattern were numbered relative to the zero cycle, and averaged to create an average OSF variation profile. The zero cycle delays relative to GM neuron burst beginning were then averaged to determine when in the gastric mill cycle the profile occurred. This technique preserved the full extent of pyloric neuron OSF changes. Maximum PY neuron OSF occurred within the GM neuron burst, whereas maximum IC and PD neuron OSF occurred during the GM neuron interburst interval. Despite these changes, pyloric cycling did not phase lock with gastric mill activity, nor were an integer number of pyloric cycles present in each gastric mill cycle. In addition to providing data necessary to predict pyloric movement, this work shows how pattern-based analysis can successfully quantify interactions between nonphase-locked networks.

2003 ◽  
Vol 89 (2) ◽  
pp. 745-753 ◽  
Author(s):  
Jeff B. Thuma ◽  
Scott L. Hooper

Cardiac sac network activity (cycle period tens of seconds to minutes) has long been known to alter pyloric network activity (cycle period approximately 1 s), but these effects have not been quantified. Some pyloric muscles extract cardiac sac timed variations in pyloric motor neuron firing, and consequently produce cardiac sac timed movements even though no cardiac sac neurons innervate them. Determining pyloric behavior therefore requires detailed description of cardiac sac effects on pyloric neural output. Pyloric muscle activity correlates well with motor neuron overall spike frequency (OSF, number of spikes per burst divided by cycle period). We therefore quantified the effects of cardiac sac activity on the OSF of all pyloric neurons in the lobster, Panulirus interruptus. The ventricular dilator (VD) neuron had a biphasic response, with its OSF first increasing and then decreasing during cardiac sac bursts. Lateral pyloric (LP) neuron OSF decreased during cardiac sac activity. The pyloric (PY) neurons had two responses, with OSF either decreasing or increasing just after the beginning of cardiac sac activity. The pyloric dilator (PD) neurons had a triphasic response, with OSF increasing slightly at the beginning of cardiac sac activity, decreasing during the cardiac sac burst, and strongly increasing after cardiac sac activity ended. The inferior cardiac (IC) neuron had a biphasic response, with OSF decreasing at the beginning of cardiac sac activity and strongly increasing when cardiac sac activity ceased. These data provide the quantitative description of cardiac sac effects on pyloric activity necessary to predict pyloric movement from pyloric neural output.


2011 ◽  
Vol 105 (1) ◽  
pp. 293-304 ◽  
Author(s):  
Bruce R. Johnson ◽  
Jessica M. Brown ◽  
Mark D. Kvarta ◽  
Jay Y. J. Lu ◽  
Lauren R. Schneider ◽  
...  

Neuromodulators modify network output by altering neuronal firing properties and synaptic strength at multiple sites; however, the functional importance of each site is often unclear. We determined the importance of monoamine modulation of a single synapse for regulation of network cycle frequency in the oscillatory pyloric network of the lobster. The pacemaker kernel of the pyloric network receives only one chemical synaptic feedback, an inhibitory synapse from the lateral pyloric (LP) neuron to the pyloric dilator (PD) neurons, which can limit cycle frequency. We measured the effects of dopamine (DA), octopamine (Oct), and serotonin (5HT) on the strength of the LP→PD synapse and the ability of the modified synapse to regulate pyloric cycle frequency. DA and Oct strengthened, whereas 5HT weakened, LP→PD inhibition. Surprisingly, the DA-strengthened LP→PD synapse lost its ability to slow the pyloric oscillations, whereas the 5HT-weakened LP→PD synapse gained a greater influence on the oscillations. These results are explained by monoamine modulation of factors that determine the firing phase of the LP neuron in each cycle. DA acts via multiple mechanisms to phase-advance the LP neuron into the pacemaker's refractory period, where the strengthened synapse has little effect. In contrast, 5HT phase-delays LP activity into a region of greater pacemaker sensitivity to LP synaptic input. Only Oct enhanced LP regulation of cycle period simply by enhancing LP→PD synaptic strength. These results show that modulation of the strength and timing of a synaptic input can differentially affect the synapse's efficacy in the network.


1998 ◽  
Vol 79 (3) ◽  
pp. 1396-1408 ◽  
Author(s):  
Stefan Clemens ◽  
Denis Combes ◽  
Pierre Meyrand ◽  
John Simmers

Clemens, Stefan, Denis Combes, Pierre Meyrand, and John Simmers. Long-term expression of two interacting motor pattern-generating networks in the stomatogastric system of freely behaving lobster. J. Neurophysiol. 79: 1396–1408, 1998. Rhythmic movements of the gastric mill and pyloric regions of the crustacean foregut are controlled by two stomatogastric neuronal networks that have been intensively studied in vitro. By using electromyographic recordings from the European lobster, Homarus gammarus, we have monitored simultaneously the motor activity of pyloric and gastric mill muscles for ≤3 mo in intact and freely behaving animals. Both pyloric and gastric mill networks are almost continuously active in vivo regardless of the presence of food. In unfed resting animals kept under “natural-like” conditions, the pyloric network expresses the typical triphasic pattern seen in vitro but at considerably slower cycle periods (2.5–3.5 s instead of 1–1.5 s). Gastric mill activity occurs at mean cycle periods of 20–50 s compared with 5–10 s in vitro but may suddenly stop for up to tens of minutes, then restart without any apparent behavioral reason. When conjointly active, the two networks express a strict coupling that involves certain but not all motor neurons of the pyloric network. The posterior pyloric constrictor muscles, innervated by a total of 8 pyloric (PY) motor neurons, are influenced by the onset of each gastric mill medial gastric/lateral gastric(MG/LG) neuron powerstroke burst, and for one cycle, PY neuron bursts may attain >300% of their mean duration. However, the duration of activity in the lateral pyloric constrictor muscle, innervated by the unique lateral pyloric (LP) motor neuron, remains unaffected by this perturbation. During this period after gastric perturbation, LP neuron and PY neurons thus express opposite burst-to-period relationships in that LP neuron burst duration is independent of the ongoing cycle period, whereas PY neuron burst duration changes with period length. In vitro the same type of gastro-pyloric interaction is observed, indicating that it is not dependent on sensory inputs. Moreover, this interaction is intrinsic to the stomatogastric ganglion itself because the relationship between the two networks persists after suppression of descending inputs to the ganglion. Intracellular recordings reveal that thisgastro-pyloric interaction originates from the gastric MG and LG neurons of the gastric network, which inhibit the pyloric pacemaker ensemble. As a consequence, the pyloric PY neurons, which are inhibited by the pyloric dilator (PD) neurons of the pyloric pacemaker group, extend their activity during the time that PD neuron is held silent. Moreover, there is evidence for a pyloro-gastric interaction, apparently rectifying, from the pyloric pacemakers back to the gastric MG/LG neuron group.


2003 ◽  
Vol 89 (3) ◽  
pp. 1327-1338 ◽  
Author(s):  
Adam L. Weaver ◽  
Scott L. Hooper

Distributed neural networks (ones characterized by high levels of interconnectivity among network neurons) are not well understood. Increased insight into these systems can be obtained by perturbing network activity so as to study the functions of specific neurons not only in the network's “baseline” activity but across a range of network activities. We applied this technique to study cycle period control in the rhythmic pyloric network of the lobster, Panulirus interruptus. Pyloric rhythmicity is driven by an endogenous oscillator, the Anterior Burster (AB) neuron. Two network neurons feed back onto the pacemaker, the Lateral Pyloric (LP) neuron by inhibition and the Ventricular Dilator (VD) neuron by electrical coupling. LP and VD neuron effects on pyloric cycle period can be studied across a range of periods by altering period by injecting current into the AB neuron and functionally removing (by hyperpolarization) the LP and VD neurons from the network at each period. Within a range of pacemaker periods, the LP and VD neurons regulate period in complementary ways. LP neuron removal speeds the network and VD neuron removal slows it. Outside this range, network activity is disrupted because the LP neuron cannot follow slow periods, and the VD neuron cannot follow fast periods. These neurons thus also limit, in complementary ways, normal pyloric activity to a certain period range. These data show that follower neurons in pacemaker networks can play central roles in controlling pacemaker period and suggest that in some cases specific functions can be assigned to individual network neurons.


1990 ◽  
Vol 64 (5) ◽  
pp. 1574-1589 ◽  
Author(s):  
S. L. Hooper ◽  
M. Moulins

1. In the lobster Palinurus vulgaris a sensory input in the lateral posterolateral nerve (lpln) of the stomatogastric nervous system (STS) is able to turn on the cardiac sac (CS) network and to induce dramatic long-lasting alterations in the output of the pyloric network. This long-lasting alteration of pyloric network output consists primarily of changes in the activity of the two neurons that innervate the muscles of the cardiopyloric valve of the stomach, with the dilator neuron (the ventricular dilator, VD) transferring from the pyloric network to the CS network and the constrictor neuron (the inferior cardiac, IC) shifting to fire earlier in the pyloric pattern. 2. The inferior ventricular (IV) neurons of the CS network make complex multiaction synaptic connections onto several pyloric neurons in a related species, Panulirus interruptus. We show that many of the short-term alterations in pyloric activity observed during CS network bursts in Palinurus are due to similar IV neuron synaptic connections. However, the long-lasting effects of lpln stimulation on pyloric output are not due to this synaptic input, because 1) direct activation of the IV neurons does not induce long-lasting changes in pyloric activity and 2) pharmacologic disconnection of this synaptic input does not abolish lpln stimulation's long-lasting effects. Lpln stimulation therefore activates two different neuronal inputs to the pyloric network. 3. The transfer of the VD neuron from the pyloric to the CS network is the result of the concerted actions of these two inputs. Lpln stimulation turns on the CS network, and the IV neurons of the CS network excite the VD neuron and ensure it fires with the CS network. The second neuronal input (that not involving known CS network neurons) abolishes in a long-lasting fashion the VD neuron regenerative (plateau) properties, and thus suppresses the ability of the VD neuron to participate in the pyloric rhythmic pattern between CS network bursts. 4. Experimental manipulation of VD neuron activity can both mimic and reverse the effects of lpln stimulation on the IC neuron. The changes in IC neuron activity are therefore not due to direct lpln-activated synaptic input onto the IC neuron, but instead are indirect "network" effects arising from the changes in VD neuron activity.


2003 ◽  
Vol 90 (4) ◽  
pp. 2378-2386 ◽  
Author(s):  
Adam L. Weaver ◽  
Scott L. Hooper

The lobster pyloric network has a densely interconnected synaptic connectivity pattern, and the role individual synapses play in generating network activity is consequently difficult to discern. We examined this issue by quantifying the effect on pyloric network phasing and spiking activity of removing the Lateral Pyloric (LP) and Ventricular Dilator (VD) neurons, which synapse onto almost all pyloric neurons. A confounding factor in this work is that LP and VD neuron removal alters pyloric cycle period. To determine the effects of LP and VD neuron removal on pyloric activity independent of these period alterations, we altered network period by current injection into a pyloric pacemaker neuron, hyperpolarized the LP or VD neuron to functionally remove each from the network, and plotted various measures of pyloric neuron activity against period with and without the LP or VD neuron. In normal physiological saline, in many (or most) cases removing either neuron had surprisingly little effect on the activity of its postsynaptic partners, which suggests that under these conditions these neurons play a relatively small role in determining pyloric activity. In the cases in which removal did alter postsynaptic activity, the effects were inconsistent across preparations, which suggests that either despite producing very similar neural outputs, pyloric networks from different animals have different cellular and synaptic properties, or some synapses contribute to network activity only under certain modulatory conditions, and the “baseline” level of modulatory influence the network receives from higher centers varies from animal to animal.


2001 ◽  
Vol 85 (4) ◽  
pp. 1424-1435 ◽  
Author(s):  
Patsy S. Dickinson ◽  
Jane Hauptman ◽  
John Hetling ◽  
Anand Mahadevan

The neuropeptide red pigment concentrating hormone (RPCH), which we have previously shown to activate the cardiac sac motor pattern and lead to a conjoint gastric mill-cardiac sac pattern in the spiny lobster Panulirus, also activates and modulates the pyloric pattern. Like the activity of gastric mill neurons in RPCH, the pattern of activity in the pyloric neurons is considerably more complex than that seen in control saline. This reflects the influence of the cardiac sac motor pattern, and particularly the upstream inferior ventricular (IV) neurons, on many of the pyloric neurons. RPCH intensifies this interaction by increasing the strength of the synaptic connections between the IV neurons and their targets in the stomatogastric ganglion. At the same time, RPCH enhances postinhibitory rebound in the lateral pyloric (LP) neuron. Taken together, these factors largely explain the complex pyloric pattern recorded in RPCH in Panulirus.


1999 ◽  
Vol 202 (7) ◽  
pp. 817-827 ◽  
Author(s):  
S. Clemens ◽  
J.C. Massabuau ◽  
P. Meyrand ◽  
J. Simmers

The well known rhythmically active pyloric neural network in intact and freely behaving lobsters Homarus gammarus was monitored prior to and following ecdysis. Despite long-lasting hormonal and metabolic alterations associated with this process, spontaneous pyloric network activity remained largely unaltered until the last 12–48 h before exuviation. At this time, the most notable change was a progressive lengthening of pyloric cycle period, which eventually attained 500–600 % of control values. It was only in the very last minutes before ecdysis that burst patterning became irregular and the otherwise strictly alternating motor sequence broke down. After the moult, coordinated rhythmicity was re-established within 10 min. Concomitant with these final changes in motor network expression at ecdysis was a drastic reduction in blood oxygen levels which led to a temporary near-anoxia. By imposing similarly deep hypoxic conditions both on intermoult animals and on the pyloric network in vitro, we mimicked to a large extent the moult-induced changes in pyloric network performance. Our data suggest that, despite major surrounding physiological perturbations, the pyloric network in vivo retains stable pattern-generating properties throughout much of the moulting process. Moreover, some of the most significant modifications in motor expression just prior to ecdysis can be related to a substantial reduction in oxygen levels in the blood.


1998 ◽  
Vol 498 (1) ◽  
pp. L51-L54 ◽  
Author(s):  
Axel Brandenburg ◽  
Steven H. Saar ◽  
Christen R. Turpin

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