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The Journal of Neurophysiology Vol. 78 No. 6 December 1997, pp. 3415-3427
Copyright ©1997 by the American Physiological Society
Graduate School Neurosciences Amsterdam, Research Institute Neurosciences Vrije Universiteit, 1081 HV Amsterdam, The Netherlands
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Jansen, Rene F., Anton W. Pieneman, and Andries ter Maat. Behavior-dependent activities of a central pattern generator in freely behaving Lymnaea stagnalis. J. Neurophysiol. 78: 3415-3427, 1997. Cyclic or repeated movements are thought to be driven by networks of neurons (central pattern generators) that are dynamic in their connectivity. During two unrelated behaviors (feeding and egg laying), we investigated the behavioral output of the buccal pattern generator as well as the electrical activity of a pair of identified interneurons that have been shown to be involved in setting the level of activity of this pattern generator (PG). Analysis of the quantile plots of the parameters that describe the behavior (movements of the buccal mass) reveals that during egg laying, the behavioral output of the PG is different compared with that during feeding. Comparison of the average durations of the different parts of the buccal movements showed that during egg laying, the duration of one specific part of buccal movement is increased. Correlated with these changes in the behavioral output of the PG were changes in the firing rate of the cerebral giant neurons (CGC), a pair of interneurons that have been shown to modulate the activity of the PG by means of multiple synaptic contacts with neurons in the buccal ganglion. Interval- and autocorrelation histograms of the behavioral output and CGC spiking show that both the PG output and the spiking properties of the CGCs are different when comparing egg-laying animals with feeding animals. Analysis of the timing relations between the CGCs and the behavioral output of the PG showed that both during feeding and egg laying, the electrical activity of the CGCs is largely in phase with the PG output, although small changes occur. We discuss how these results lead to specific predictions about the kinds of changes that are likely to occur when the animal switches the PG from feeding to egg laying and how the hormones that cause egg laying are likely to be involved.
In the past decade, it has become clear that many pattern-generating networks are not fixed, specialized units that only drive one single motor act, but rather dynamic networks of neurons that can be modified and reconfigured to generate different patterns of output (Weimann et al. 1991 Animals
All experiments were done in vivo using freely behaving pond snails (Lymnaea stagnalis). Adult specimen age 4-6 mo, shell length 25-35 mm, bred under standard laboratory conditions were used in all experiments. The animals were housed in perforated jars placed in a large tank with running fresh water (20°C) and were kept under a 12 h-12 h light-dark cycle and fed a daily ration of lettuce.
Fine-wire recording of CGC cell bodies and cerebro-buccal connectives
Permanently implanted electrodes were used to monitor electrical activity in connectives and cell bodies in freely behaving animals (Parsons et al. 1983 Analysis of behavior
Buccal rasping was analyzed from videotape and frame-by-frame photographs. The buccal movement has been described by Benjamin (Benjamin et al. 1985
Recording and analysis of electrical signals
Electrical activity recorded with fine-wire electrodes was fed through a WPI DAM-80 differential amplifier and stored on the hifi-track of the video tape used to store the recording of the animals' behavior. A time-code generator (VITC, Alpermann and Velte, Wuppertal, Germany) was used to provide every video frame with a time code to be able to synchronize the behavior stored on videotape with the digitized electrical activity of nerves, connectives or cell bodies. The electrical activity was digitized using a Cambridge Electronic Design model 1401 or 1401Plus, 12-bit A/D converter that was running a special wavecapture protocol (see Jansen and ter Maat 1992
Permutation tests
The correlation between CGC spiking and buccal rasping movements was investigated by means of permutation tests. Permutation tests have been used to investigate patterns in spike trains (Dayhoff and Gerstein 1983 Egg-laying-related rasping movements are different from feeding movements
Our first aim was to come to a qualitative and quantitative description of the behavioral output of the buccal system during the two behaviors under investigation, feeding and egg laying. Feeding movements of Lymnaea in the past have been described as a four-phase rhythm (protraction, rasp, swallow, and inactive) (Benjamin et al. 1985
CGC neurons are electrically active during spontaneous egg laying
It has been shown that the differences in firing pattern and frequency between CGCs recorded neurons in freely behaving animals and in isolated central nervous systems are appreciable. In the intact animals, for example, firing rates are 10-fold lower than in the isolated CNS (Yeoman et al. 1994
Firing pattern of the CGCs during egg laying is different from that during feeding
On the basis of behavioral experiments, a firing rate of 6.7 action potentials/min has been proposed to be the minimum rate of CGC firing that still allows the feeding pattern generator to work in freely behaving animals (Yeoman et al. 1994
CGC firing is suppressed during the rasp phase of
egg-laying-related rasping movement
Although there obviously is no one-for-one relationship between CGC spikes and rasping movements of the buccal mass in feeding animals (Figs. 6 and 7), Yeoman et al. (1994)
In this paper, we have investigated the activities of the CPG and a pair of associated higher order interneurons (CGCs) during two unrelated behaviors (feeding and egg laying). We have found that there are differences between the motor patterns expressed during the two behaviors. The results show that the CGCs are involved in the modulation of the buccal pattern-generator system during feeding and during egg laying. However, the timing relation between the CGC spikes and the cycle of the buccal CPG changes little, and additional modulating factors are needed to explain the observed differences in motor patterns.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). Hormones, neurotransmitters as well as individual neurons have been shown to be able to modify ("rewire") existing networks of neurons or form entirely new networks (Dickinson et al. 1990; Hooper and Moulins 1989). Most of these modifications involve the modulation of membrane and synaptic properties of neurons in the network (Hooper and Moulins 1989). These mechanisms are thought to enable an animal to control different behaviors (or different aspects of a single behavior) using just a small number of neurons.
showed that pattern-generating neurons switch their patterns of electrical activity during different movements of the gastric mill cycle. The critical difference between preparations and intact animals is, obviously, that in intact animals, the output of pattern-generating networks depends on sensory input (Barnes and Gladden 1985). Many pattern-generating networks, however, have been studied in the absence of the normal sensory signals (isolated central nervous systems, reduced preparations). This absence of sensory information makes it very difficult to predict the properties of networks of neurons in intact animals from observations made in vitro.
; Benjamin et al. 1979, 1985; Yeoman et al. 1994). Benjamin and colleagues have described extensively the pattern-generating network that drives motor neurons of the feeding apparatus. This feeding pattern generator is composed of three types of interneurons that can be driven by a slow oscillator neuron. The interneurons fire in sequence to produce a four-phase rhythm (protraction, rasp, swallow, and inactive) (Benjamin et al. 1985) that drives the motor neurons. The feeding pattern-generating network is modulated by identified higher order neurons that are located in the cerebral ganglia (McCrohan 1984; McCrohan and Audesirk 1987; Yeoman et al. 1994). Among these are the serotonergic cerebral giant cells (CGCs), a pair of neurons that is homologous to the metacerebral neurons that are associated with the feeding systems of other gastropods (Granzow and Kater 1977).
). Similar long-lasting effects are seen after application of the transmitter serotonin. In the past, it has been hypothesized that the CGCs have command neuronlike properties (McCrohan 1984; McCrohan et al. 1987), but it recently has been shown that electrical activity of the CGCs does not directly cause feeding movements: experiments in freely behaving animals showed that during feeding, the CGCs fire at a specific minimum rate (Yeoman et al. 1994). Higher rates of firing of the CGCs than this threshold level are thought to set the rate of the feeding cycle.
). During the turning and oviposition phases of egg laying (ter Maat et al. 1986) the animal makes frequent rasping movements with the buccal mass. As opposed to feeding, however, it does not appear to collect food with this activity (Goldschmeding et al. 1983). During egg laying on a leafy substrate such as lettuce, only the topmost layer of cells is removed, and it is thought to allow for the proper attachment of the egg mass that is about to be deposited. When the animal is made to lay eggs on a starch covered glass plate, the rasping movements remove the starch only from the location where the egg mass is to be deposited (Goldschmeding et al. 1983). Egg-laying-related rasping also occurs on a completely clean substrate such as glass. When rasping is prevented by lesions of the cerebrobuccal connective, the egg mass is not attached to the substrate properly and frequently ends up on the bottom of the tank (Ferguson et al. 1993).
). When this nerve is cut, egg-laying-related rasping does not occur but feeding is unaffected (Ferguson et al. 1993). Egg-laying-related rasping is caused, either directly or indirectly, by peptides released from the neuroendocrine cells in the CNS that trigger egg laying, the caudodorsal cells (CDCs). The CDCs express two CDCH genes (Vreugdenhil et al. 1989) and release a number of different peptides to the blood and to the CNS (Li et al. 1994) during a discharge of electrical spiking activity that occurs ~2 h before egg laying.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). The procedures were as described by Hermann et al. (1994) for nerve and connective recordings and by Yeoman et al. (1994) for cell body recordings. In short, stainless steel wire electrodes (25 µm diam, California Fine Wire) were implanted to record electrical spiking activity. Animals were anaesthetized by injection of 1.5 ml of MgCl2 (50 µl) into the foot. The head-foot was opened dorsally over a length of 3 mm. In the case of cell body recordings, the outer connective tissue layer that overlies the cell bodies was removed carefully. Next, electrodes were inserted into the body cavity through the body wall and the insulation of the end of the fine wire was removed over a length of ~200 µm. The bare end of the wire was bent into a circle. The plane of the circle then was bent again to make an angle of 90° to the rest of the wire and glued into place by means of superglue (Pattex, Nieuwegein, The Netherlands). In the case of nerve and connective recordings, electrodes were inserted into the body cavity through the body wall and positioned around the nerve or connective. The tissue was dried with a jet of air, and the wire was secured with tissue adhesive (cell bodies) or with dental impression material (Reflect, Kerr) in the case of nerves and connectives.
) as the sequence protraction, rasp, swallow, and inactive. In intact animals, the swallowing movement is not visible and we thus used the terms "open," "rasp," and "closed." In this study, open and rasp presumably correspond to protraction and retraction, respectively, of the radula. As mentioned earlier, the swallowing movement is not visible in intact animals and is included in the closed phase.
). The durations of these behaviors are, however, variable. The start of resting phase of egg-laying behavior was identified by the start of the discharge of the CDCs, the neuroendocrine cells that trigger egg laying (ter Maat et al. 1986). The massed low-frequency electrical activity of the CDCs that marks the start of the CDC discharge of spikes of these neurons in most animals can be made visible in the signal recorded from the electrodes implanted on the CGC neurons by filtering the signal (see further). The onset of the turning and oviposition phases of the egg-laying behavior are determined by the overt behavior of the animals as described earlier (ter Maat et al. 1986). Interval distributions (Figs. 1 and 2) are shown as quantile plots (Systat, Evanston, IL).
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FIG. 1.
Interval distributions of the open and the rasp phase of the rasping movement. A: quantile plots of the interval distribution of the open in a feeding animal. Graph shows the open times measured (x axis) plotted against the proportion of the data with that value (y axis). Dashed line, linear regressions of the log-survival data points. B: log-survival plot of the data shown in A. A single exponential with no lag-time would have resulted in a log-survival plot that shows a straight line through the origin. Systematic deviations from a straight line indicate that mixture of multiple exponential distributions is present. When the plot is (nearly) horizontal for small values of x, a lag-time is indicated (see Haccou and Meelis 1992 ). C: quantile plots of rasp in a feeding animal. D: log-survival plot of the data shown in C.
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FIG. 2.
Difference in interval distributions of the closed phase between feeding (A and B) and egg-laying (C and D) animals. A: quantile plots of the interval distribution of the closed state in a feeding animal. B: log-survival plot of the data in A. C: quantile plots of the closed times in an egg-laying animal. D: log-survival plot of the data shown in C. Interval distributions of the closed times were single exponentials in 5 of 6 egg-laying animals. In feeding animals, the interval distributions were composed of multiple exponentials (see text for details).
). During digitization, both the waveform activity as well as the matching VITC signal are read from tape.
). During this discharge, the CDCs fire in near unison, and the electrical signal of the ~100 CDCs firing in concert is large enough to be picked up at the CGC soma site.
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FIG. 4.
Electrical activity recorded from the soma of a cerebral giant neuron during egg laying in a freely behaving animal. A: slow runout of the electrical activity recorded from the soma of a cerebral giant cell (CGC). Large spikes stand out against the background. Large arrow on the left indicates the starting point of the faster runout shown in B. B: faster runout of A, indicated by the large arrow in A. Filtering of this signal (see METHODS) reveals the onset of the burst discharge of electrical spiking activity of the caudodorsal cells, also located in the in the cerebral ganglion. This burst discharge marks the start of egg laying. C: histogram of the electrical activity of the CGC before, during, and after egg laying. Note that the histogram in C shows a longer piece of the recording than A does.
), the relation among spike trains (Lindsey et al. 1992), and behavioral data (Adams and Anthony 1996). Similar tests are used in randomization tests for single subject experiments (Edgington 1995; Edgington and Bland 1993). True randomization tests, however, rely on the random assignment of treatments to time blocks. In this paper, we are investigating spontaneous behavior, and consequently is it impossible to assign randomly treatments to time blocks.
2
ln p of n independent P values follows a 
2 distribution with 2n df (Fisher 1932; Sokal and Rohlf 1995). All the results of permutation tests presented here are based on 10,000 random permutations. The random number generator used is a long period (>2*1018) generator (Press et al. 1992).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
). Although it is debatable whether "inactive" can be called a genuine phase of any pattern generator without the definition becoming self-referential, we include this phase in our description of the behavior.
). The result was significant (P < 0.05) for all feeding animals and one of six egg-laying animals. This shows that in five of six egg-laying animals the closed bouts had a single exponential distribution. This indicates that the likelihood that an egg-laying animal ended a closed bout (by starting a rasping movement) was constant and thus can be considered as one single behavioral process. The closed bouts in feeding animals were composed of a mixture of exponentials. Also, the closed bouts were much shorter during feeding than during egg laying.
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FIG. 3.
Average lengths of the open and rasp phases of the rasping movement in egg-laying (left) and feeding animals (right). Duration of the open phase was significantly shorter in feeding animals (*).
). To investigate the role that the CGCs play in modulating the buccal system during egg laying, we therefore first needed to establish whether or not the CGCs are active at all during egg laying.
; Jansen et al. 1996). The cell bodies of CGC neurons also are identified easily because they are the largest ones on the ventral side of the anterior part of the cerebral ganglion (diameter 100-200 µm).
). At the start of the resting phase, no immediate changes in the firing rate of the CGC occurred, but in most animals, the firing rate of the CGCs slowly decreased during the course of 5-10 min. In the example shown, the onset of egg laying was determined by the start of the discharge of the CDCs (see METHODS and Fig. 4B). About 10 min after the start of the resting phase, the average firing rate of the CGC dropped to ~20 spikes/5 min (Fig. 5, A and B). When counted as the total number of spikes that occurred in the 20-min periods just before and after the start of the resting phase, the firing rate of the CGCs rate was significantly lower after the start of the resting phase (square root transformed, t-test, P = 0.027, n = 5).
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FIG. 5.
Average spiking activity of the CGCs of 5 animals. A: recordings were aligned around the end of the oviposition phase of the egg-laying behavior. Average onset ± SE of each of the 3 phases of egg-laying behavior (resting, turning, and oviposition) are shown. B: spiking of the CGCs around different transition moments in the egg-laying behavior. Spiking activity was counted as the total number of spikes in 20 before and after a transition. Both at start of resting and at the end of oviposition, a significant drop in the electrical activity of the CGCs was seen.
). This shows that the CGC neurons are active during the turning phase, when egg-laying-related rasping occurs.
). The current data show that during the last 20 min of the turning/oviposition phases of egg laying, the firing rate of the CGCs was 6.45 spikes/min (129 spikes/20 ± 33.7 min, Fig. 5B). This would be just below the rate needed to enable the feeding rhythm generator to oscillate. Because the animals make frequent rasping movements during this phase of egg-laying behavior, this suggests that alternative mechanisms may play a role. However, because the overall firing rate of a neuron gives no information about its firing pattern, we investigated the firing patterns of the CGCs during feeding and egg laying as well as the patterns of buccal activity during both behaviors.
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FIG. 6.
Interval- and autocorrelation plots of buccal rasping and CGC spiking during feeding. A: interval histograms of rasping (top) and CGC spiking (bottom) are shown on the left, the autocorrelation histograms on the right top and bottom. B: chart recorder output of CGC spiking (top) and the buccal rasping. Behavioral categories, from top to bottom, are closed, open, rasp, and invisible. Latter is not a part of the rasping movement per se, but is used to indicate the periods that the mouth of the animal is obscured by food.
). In the case of rasping, the moment of the transition closed-open (the start of the feeding movement) was used to construct the histograms. The results are shown in Figs. 6 and 7.
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FIG. 7.
Interval- and autocorrelation plots of buccal rasping and CGC spiking during egg laying. A: interval histograms of rasping (top) and CGC spiking (bottom) are shown on the left, the autocorrelation histograms on the right top and bottom. B: chart recorder output of CGC spiking (top) and the buccal rasping (feeding animal). Behavioral categories, from top to bottom, are closed, open, and rasp. Invisible did not occur during egg laying.
describe that in feeding animals CGC spikes were "phase locked to the feeding movements of the animal" and that no CGC spikes occur during the bite itself. However, no quantitative data are available.
have shown that the CGCs make monosynaptic connections with neurons in the buccal ganglia, with postsynaptic effects in the buccal neurons ranging from tens of milliseconds to 10 s. We therefore investigated quantitatively whether a relation exists between the firing of the CGCs and the rasping cycle of the buccal system in feeding and egg-laying animals.
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FIG. 8.
Cross-correlation plots of buccal rasping and CGC spiking during feeding (A and B) and egg laying (C and D). A: records of CGC spiking in a feeding animal were aligned at the occurrences of the behavioral transition from closed to open. Each CGC spike within the 20 + 20 s window is marked by a vertical line within the horizontal lane that indicates that particular transition. B: individual CGC spikes are added across transitions and are shown in a histogram (bin size = 0.4 s). Transition closed-open coincided with high CGC spiking activity. C: as in A but now for an egg-laying animal. D: histogram of the data shown in D. Although the overall spiking activity is lower than in feeding animals, the transition closed-open also coincided with (relatively) high CGC spiking activity.
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FIG. 9.
Permutation test of the relation between CGC spikes and the closed, open, and rasp phases of the rasping movement. A: top 2 traces (marked CGC spikes and Original behavior) show the original arrangement of CGC spikes and rasping behavior. CGC spikes that occur during each of the phases are counted. Bottom 2 traces show 2 examples of permuted sequences. B: result of the permutation test for the rasp phase. Almost all of the 10,000 randomly permuted sequences result in a CGC spike count higher than that of the original sequence, indicating that it is unlikely that is was obtained by chance.
View this table:
TABLE 1.
2 values for combined probabilities
describe that CGC spikes occur "just before the opening of the mouth" in feeding animals. To investigate this quantitatively in feeding and egg-laying animals, a second permutation test was done.
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FIG. 10.
Permutation test of the relation between CGC spikes and specific parts of the rasping movement. A: top 2 traces show the original arrangement of CGC spikes and rasping behavior. CGC spikes that occur a period that precedes the transition closed-open are counted. Bottom 2 traces show 2 of the 10,000 permuted runs, where the counting periods are arranged at random. B: result for a counting period of 3 s before the transition closed-open. Large majority of the 10,000 permuted runs had a total spike count lower than the original period. This indicates that it is unlikely that that the original count was high by chance.
View this table:
TABLE 2.
2 values for combined probabilities
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Possibly this low spontaneous firing rate of the CGCs helps to suppress the buccal CPG during the resting phase. During the turning and oviposition phases, CGCs are active, and it is during this phase that the animal shows buccal rasping activity (ter Maat et al. 1986). This correlation suggests that the activity of the CGCs may be necessary for the expression of the buccal CPG during egg laying. The latter also is borne out by the fact that CGC activity drops off significantly at the end of oviposition.
). The distributions of the duration of all three elements of the rasping movement (open, rasp, and closed) all had a lag-time that was greater than the time-resolution of the measurement. This indicates that all three have a certain minimum duration that probably represents the minimum time the animals needs to make the movement. The duration of both open and rasp followed a distribution that was characterized by multiple exponentials. This indicates that open and rasp are composed of multiple acts that each are distributed exponentially (Haccou and Meelis 1992). The distributions of closed bouts in egg-laying animals were distributed as a single exponential, which indicates that in these animals, closed can be considered as one single act that has a constant chance of being terminated (by a rasping movement). In all feeding animals, the distribution of the closed bouts contained multiple exponents, and this suggests that, in feeding animals, closed cannot be considered as a single act, but that it is composed of multiple components.
).
. These authors investigated fictive feeding in starved animals that were fed just before the experiment, and they distinguished two different feeding rhythms: spontaneous and slow oscillator (SO) driven. The SO is an unpaired identified neuron, which on depolarization starts the buccal pattern generator (Rose and Benjamin 1981). These two rhythms were different with regard to the sources of the variability of the relative timing of the generated rhythm. In the spontaneous rhythm, the N3 phase (swallow) was the only variable phase, whereas in the SO-driven rhythm, both the N1 phase (protraction) and N3 were variable. In all cases, the N2 phase (rasp) was relatively fixed. The open phase most likely corresponds with the protraction movement of the radula, which is driven by the N1 neurons of the CPG. Because the length of the open phase was increased by ~50% during egg laying, it is possible that this is caused by circulating or locally released CDC peptides. These N1 neurons have bursting properties, and it is tempting to speculate that the longer open phase seen during egg laying is caused by CDC-peptides changing the bursting properties of these N1 neurons.
; McCrohan and Kyriakides 1989), but also the unpaired buccal SO neuron can trigger the motor program (Rose and Benjamin 1981). Firing the CGCs at very high rates also can trigger the motor program, but these rates have never been seen in the intact animal (Yeoman et al. 1994; this study). Instead, the CGCs now are thought to play a modulatory role: firing rates >6.7/min enable the feeding motor program, and rates between 6.7 and 20/min influence the rate of the motor program cycle (Yeoman et al. 1994).
). Second, one of the visceral nerves that innervates the female tract (the intestinal nerve) is necessary and sufficient for the buccal rasping (but not feeding itself) to occur during egg laying. Furthermore, recordings from the intestinal nerve in freely behaving animals have shown electrical activity correlated with rasping activity (Jansen and ter Maat, unpublished data). An alternate additional source of excitation of the buccal pattern generator could be peptides from the CDCH gene (which also encodes for the ovulation hormone itself). Van Minnen et al. (1988) have shown that neurons that stain positive with a monoclonal anti-CDCH antibody are found in the buccal ganglia. This shows that the CDCH-1 gene is expressed in neurons in the buccal ganglia and suggests that local release of peptides encoded on this gene may play a role in the modulation of the buccal pattern generator during egg laying.
; Dayhoff and Gerstein 1983; Lindsey et al. 1992). Translating the effects measured in individual tests to effects at the population level was done by using a statistical method (Fishers test for multiple independent P values) from the field of meta-analysis (Hedges and Olkin 1985).
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FOOTNOTES |
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Address for reprint requests: R. F. Jansen, Faculty of Biology, Graduate School of Neurosciences Amsterdam, Research Institute Neurosciences Vreje Universiteit, 0181 HV Amsterdam, The Netherlands.
Received 3 December 1996; accepted in final form 15 August 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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