higher order neurons in the cerebral ganglia ofpleurobranchaea have diverse effects on buccal motor...

J Comp Physiol (1983) 153:533-541 Journal of Comparative Physiology. A �9 Springer-Verlag 1983

Higher order neurons in the cerebral ganglia of Pleurobranchaea have diverse effects on buccal motor patterns

Andrew D. McClellan* Department of Anatomy and Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106, USA

Accepted August 9, 1983

Summary. Structures of the buccal mass (radula, jaws, and lips) of the gastropod Pleurobranchaea are used during several behaviors: feeding (ingestion and swallowing phases), regurgitation (writhing and vomiting phases), and rejection. In so far as the ' command ' neurons for the above behaviors are largely unknown, the present study examined the diversity of motor patterns elicited by 'de- scending' neurons in the cerebral ganglia and the relationship of these cells to vomiting motor activity, which can be identified in isolated preparations.

Stimulation of metacerebral giant cells (MCG) elicited a relatively weak motor pattern of uncer- tain function. The activity in these cells was sup- pressed during vomiting rhythms.

Stimulation of different paracerebral cells (PC) elicited motor activity that differed in both intensity and pattern, and some PC cells were inhibitory. Stimulation of 20% of the excitatory PC cells in combination with on-going motor activity elicited vomiting-like motor patterns. Approximately 38% of all PC cells fired bursts during vomiting rhythms. The results suggest that the PC cells are part of a heterogenous group of neurons, and are activated in different combinations to produce variations in motor activity and behavioral function.

Introduction

It has been known for some time that electrical stimulation of single ' command ' neurons (Hughes

* Present address: Department of Physiology, School of Medi- cine, University of North Carolina, Chapel Hill, North Caro- lina 27514, USA

Abbreviations: CBC cerebrobuccal connective; MCG metacerebral giant cells; M N mouth nerve; PC paracerebral cells; SD salivary duct; SO VN small oval veil nerve

and Wiersma 1960; Davis 1977; Kupfermann and Weiss 1978) can elicit motor patterns which underlie complete behaviors (Wiersma 1938; Kennedy et al. 1966; Willows 1967; Atwood and Wiersma 1967; Zucker et al. 1971; Larimer et al. 1971), while other cells are apparently active as a group because alone they only elicit part of the motor activity of a particular behavior (Wiersma and Ike- da 1964; Evoy and Kennedy 1967; Kennedy et al. 1967; Larimer and Kennedy 1969; Davis and Ken- nedy 1972a, b; Bowerman and Larimer 1974a, b).

In the gastropod Pleurobranchaea, structures of the buccal mass (radula, jaws, and lips) are rhythmically active in different coordination patterns during several behaviors: feeding (ingestive and swallowing phases), regurgitation (writhing and vomiting phases) of visceral irritants (e.g. soap solution), and rejection of unpalatable, inert objects (e.g. string, rubber tubing) (McClellan 1978, 1982a). In other studies, ' ingestion' was used as a general term for feeding (unspecified phase), while the term' egestion' was applied to both rejection and the vomiting phase of regurgitation (Croll and Davis 1982). The isolated nervous system of Pleurobranchaea can be made to generate two buccal motor patterns which alternate: (a) a ' primary' rhythm which involves a response thought to be part of either swallowing (feeding) or the writhing phase (regurgitation), and which therefore cannot presently be uniquely correlated with a single behavioral function (also verified by Croll and Davis 1982), and (b) periodic bouts of an unambiguous vomiting rhythm (see Methods; McClellan 1979, 1982b). Both of these rhythms involve alternating buccal root activity, the neural correlate of rhythmic radula movement (McClellan 1982b).

Although several groups of higher order neurons in Pleurobranchaea have been shown to activate alternating buccal root activity when stimulated (Davis ~977), the ' command ' neurons for

534 A.D. McClellan: Diversity of cerebral ganglia neurons in Pleurobranehaea

the above behaviors are largely unknown. Some of the higher order neurons in the buccal ganglia have recently been shown to activate vomit ing motor pat terns, which include al ternat ing buccal roo t activity (McClel lan 1979, 1983). In the present study, higher order neurons (metacerebral giant cells and paracerebra l cells) in the cerebral ganglia were st imulated singly and the elicited m o t o r patterns recorded in isolated nervous systems to determine the diversity o f these neurons and if they might act together in p roduc ing different m o t o r functions. Also, the relat ionship o f these cells to vomit ing m o t o r activity was examined. A previous study examined the role o f higher order neurons in the buccal ganglia (McClel lan 1983).

Materials and methods

Isolated nervous system preparation. All experiments were performed with the isolated nervous system, which consisted of all major ganglia and the attached salivary duct (for anatomical organization, see Fig. 7 in McClellan 1982b). Primary rhythms, which were periodically interrupted by brief episodes of vomiting rhythms, were elicited by stimulating esophageal nerves (1 ms constant current pulses at 1 Hz), as previously described (McClellan 1982b). Both rhythms consisted of alternating activity in buccal roots one (R1 activity produces radula protrac- tion) and buccal root three (R3 activity produces radula retrac- tion). The salivary duct (SD) was phasically active during primary rhythms but was inactive during vomiting rhythms. A cerebral root, the mouth nerve (MN; mainly produces mouth opening), was largely active during R3 bursts during primary rhythms, but was tonically active during vomiting rhythms. A second cerebral root, the small oral veil nerve (SOVN; mainly produces withdrawal of the oral veil), was largely active in phase with R3 bursts during primary rhythms, but was active in phase with the end of R1 bursts or was tonically active during vomiting patterns.

When elicited in semi-intact preparations by esophageal nerve stimulation, the primary and vomiting rhythms were clearly distinguished. The primary rhythm was manifested in a response and pattern of muscle activity similar to that occurring during swallowing (phase of feeding) or writhing (the non- expulsion phase of regurgitation). These latter two behavioral responses appeared similar and could perhaps both function to remove material from the esophagus (i.e. swallowing), but for different reasons (see McClellan 1982b, for a discussion concerning the function of the primary rhythm). In contrast, the vomiting rhythm was accompanied by unambiguous expulsion. Both rhythms involved rhythmic radula movement (McClellan 1979, 1980, 1982b). Similar results were found by Croll and Davis (1982).

Neurophysiology. The above components of the motor patterns were recorded extracellularly with conventional suction electrodes. Intracellular recording and stimulation was performed with double-barrelled glass microelectrodes filled with 3 mol/1 KC1 and having d.c. resistances of 10-50 Mr2. Electrodes were sharpened with a jet-stream beveler to improve their current passing properties (Ogden et al. 1978). Recording and stimulation were done with a recording amplifier which had an active current source and electronic bridge (Colburn and Schwartz 1972; McClellan 1981). Details of the recording techniques,

instrumentation, and data management were presented else- where (McClellan 1982a, b).

Cobalt staining. The previously reported positions of metacerebral and paracerebral neurons in the cerebral ganglia (Davis 1977) were verified by cobalt back-fills of the cerebrobuccal connective (CBC) using the 'Wick technique' (Kater et al. 1973), as previously described (McClellan 1983).

Results

The basic p ro toco l was to stimulate singly the metacerebral giant ( M C G ) cells or the paracerebral (PC) cells and record the elicited m o t o r pa t te rn not only in buccal roots R3 and R1, but also in the SD, M N , and SOVN. In addit ion, these cells were recorded f rom during pr imary and vomit ing rhythms, which were elicited by esophageal nerve st imulat ion (see Methods) , in par t icular to determine if some cells were act ivated or inhibited during vomit ing rhythms. Finally, all cells were stimulated during buccal m o t o r activity in order to re- veal possible inhibi tory effects or to determine if these neurons could switch the pa t te rn to bouts o f a vomit ing rhythm. These manipula t ions were largely concerned with the relat ionships o f the two groups of neurons with vomit ing and are relevant, since prel iminary experiments with behavioral ly re- sponsive semi-intact animals indicated that during vomit ing the M C G s were inhibited while some of the PC cells became active (McClel lan 1980, un- published).

Metacerebral giant cells ( M C G )

The two large M C G cells were identified by their locat ion in each anter ior lobe o f the cerebral ganglia, and by the electrophysiological demons t ra t ion of axons in the ipsilateral cerebrobuccal connect ive (CBC) and m o u t h nerve (MN) (Gillette and Davis 1977). A total o f 18 cells were examined in 15 preparations.

In quiescent preparat ions , s t imulation o f one or bo th M C G cells at m a x i m u m physiological frequencies (i.e. 1-2 Hz; Gillette and Davis 1977) elicited at best only one cycle o f weak and variable m o t o r activity which started with a R1 burst and was fol lowed by a R3 burst. St imulat ion at somewhat higher frequencies could elicit one or perhaps two cycles o f modera te ly intense m o t o r activity (Fig. 1 A; see Fig. 8, Gillette and Davis 1977). Dur- ing the elicited m o t o r pat terns the SD was often inactive, but since the M N and SOVN were only weakly active and the m o t o r activity was weak the elicited pat terns could no t be considered to underlie vomit ing (see Methods) .

A.D. McClellan : Diversity of cerebral ganglia neurons in Pleurobranchaea 535

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Fig. 1. A Motor activity elicited in quiescent isolated preparations by depolarization and high frequency spiking of MCG cells. One or two cycles of alternating activity in buccal roots (R1 and R3) is accompanied by variable activity in the SD. Activity in cerebral roots (SOVN and MN) is weak. B, C MCG stimulation during primary rhythms, elicited by esophageal nerve stimulation (see Methods). B Tonic depolarization and increased firing of the MCG (right section of record) accelerates the on-going primary rhythm but does not alter the pattern. C Pulsed depolarization and spiking of the MCG affects the timing of the on-going primary rhythm (note that seven of the nine R3 bursts are essentially phase-locked to the fourteen MCG bursts in a 1:2 relationship). D Recording of MCG activity during motor patterns elicited by esophageal nerve stimulation. During a primary rhythm (left and right) the MCG cell fires at a relatively low frequency, while during vomiting rhythms (between arrows) the cell is partially or completely inhibited

During an on-going primary rhythm (elicited by esophageal nerve stimulation; see Methods), tonic depolarization and spiking of single MCGs could briefly accelerate the motor activity (Fig. 1 B; right). Pulsed stimulation of the MCG could affect the timing of the primary rhythm (Fig. 1 C; note that seven of the nine R3 bursts were phase-locked to the fourteen MCG bursts in a 1:2 relationship). When the MCG bursts were elicited at a higher frequency, a 1:1 entrainment with the motor rhythm could result (Gillette and Davis 1977). In all cases, the pattern of the on- going rhythm did not appear to be altered by MCG stimulation. It should be noted that stimulation of about half the cells had much weaker effects than shown here.

During primary rhythms, about 50% of the MCGs fired action potentials at between 0.05-1.0 Hz (Fig. 1D, left and right sections), while the remaining cells were essentially silent. MCG spikes were sometimes phase-locked to the

rhythm (Fig. 1 D) as previously reported (Gillette and Davis 1977). During periodic episodes of vomiting rhythms (Figs. I D, between arrows; see Methods), the MCG spikes were reduced in frequency or totally inhibited.

Paracerebral cells (PC)

The PC cells have been anatomically defined as a group of about 10-15 interneurons which are located on the dorsal surface of the cerebral ganglia within about a 100 ~m radius of the base of each tentacle nerve and which have axons in the ipsilateral CBC (see Fig. 3 in Davis 1977). In previous studies only some of the PC cells were examined because they were required to satisfy three and sometimes four of the following criteria: (a) a specific location of the cells (however, see below); (b) electrophysiological demonstration of a 'de- scending' axon in the ipsilateral CBC; (c) the abili- ty to initiate ' s t rong' motor activity when stimu-

536

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A.D. McClellan: Diversity of cerebral ganglia neurons in Pleurobranchaea

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Fig. 2A-D. Sample of the types of motor patterns elicited by tonic depolarization and high frequency spiking of PC cells during quiescent conditions in isolated preparations. A, B Two different PC cells initially activate strong motor patterns which decrease in intensity during the period of stimulation. Buccal root activity (R3 and RI) and SD activity is similar in both records, but the cerebral root activity (SOVN and MN) is stronger in B. C A relatively weak (note time scale) and erratic motor pattern elicited by a PC cell. D Example of an extremely weak motor pattern, elicited by PC cell stimulation, which included little cerebral root activity (SOVN)

lated; and (d) a specific pattern of periodic synaptic inhibition (Gillette et al. 1978). Since all PC cells were of interest in the present study, all candi- date cells were only required to satisfy the first two of the above criteria (i.e. general location and 1:1 antidromic/orthodromic activation via the CBC). Two sub-populations of PC cells were found, one located predominantly near the base of the tentacle nerve (excitatory group) and an- other group located slightly anterior to this (inhibitory group). Unfortunately, it was difficult to compare the present results with those previously published because the third criterion was vague, it was unclear how many of the cells satisfied the fourth criterion, and a smaller part of the elicited motor activity was recorded. In the present study, a total of 40 PC neurons were examined in 13 preparations.

In any given preparation, different PC cells could be distinguished on the basis of location, the shape of orthodromic spikes in the CBC, and

by the effects on motor activity from stimulating the cell (e.g. Fig. 3; PC3, PC6, and PC7 are from the same preparation). Inter-preparation compari- sons of PC cells were more qualitative, because the units in a given nerve recording often have different relative amplitudes in different preparations. Thus, in different preparations it is sometimes difficult to identify similar motor activity, except for vomiting patterns.

In quiescent preparations, intercellular depolarization resulting in high frequency firing of different excitatory PC cells elicited motor activity that differed in both intensity and pattern. Stimu- lation of 15% (6 of 40) of the PC cells elicited relatively strong motor activity which had cycle times less than 10.0 s (Fig. 3A, C), 25% (10 of 40) of the cells elicited patterns with moderate cycle times (10-20 s), while 25% (10 of 40) of the neurons activated rather weak or erratic motor patterns with cycle times greater than 20.0 s (Fig. 2 D). The intensity of the elicited patterns sometimes de-

A.D. McClellan: Diversity of cerebral ganglia neurons in Pleurobranchaea 537

creased during PC cell stimulation (Fig. 2A, C). Approximately 35% (14 of 40) of the PC cells did not elicit motor activity when stimulated, but 70% of these cells were located in the secondary group which contained inhibitory PC cells (see below and Fig. 3 E).

The motor patterns elicited by stimulation of excitatory PC cells invariably began with a burst in R1, which would normally produce radula pro- traction (Davis et al. 1973), followed by clear recip- rocal activity in R3 and R1. The structure of the elicited cycles was either symmetrical (59%) (Figs. 2D, 3A, C) or skewed towards prolonged R3 bursts (32%) (Fig. 2A, B). The SD was active during 76% of these motor patterns, but occa- sional inactivity in this component was not neces- sarily dependent on the elicited pattern or its intensity (compare Figs. 2 D, 3 A).

During stimulation of different excitatory PC cells, the differences in buccal root activity (R3 and RI) were only moderate, while in contrast the activity in cerebral roots varied considerably in both intensity and pattern, as also noted by others (Cohan 1980; Cohan and Mpitsos 1983). The PC cells elicited motor patterns in which MN activity could be tonic (18%), in phase with R3 bursts (73%), or in phase with R1 bursts (9%). During these same evoked patterns, SOVN activity could be tonic (29%), in phase with R3 bursts (19%), or in phase with R1 bursts or the R1-R3 transitions (52%). As a rule, the patterns in these two cerebral roots were both tonic or both phasic.

Each excitatory PC cell was also stimulated during on-going primary rhythms (elicited by esophageal nerve stimulation; see Methods) in order to determine if the pattern could be modified or inhibited. Stimulation of the excitatory types of cells described above during on-going rhythms produced three types of results: (a) no effect - 30%; (b) an acceleration but not a change in the pattern - 10%; and (c) slight modifications of the on-going pattern - 60% (12 of 20). In the last case, the modified motor patterns usually resembled the motor activity elicited by the particular cell during quiescent conditions. However, stimulation of 20% (4 of 20) of the excitatory PC neurons modified the on-going primary rhythm so that it was partly novel and resembled a vomiting motor pattern (McClellan 1980). For example, stimulation of one of the PC cells during quiescent conditions elicited a pattern with phasic MN and SOVN activity (Fig. 3 A), while the same cell stimulation applied during a primary rhythm accelerated the pattern and resulted in tonic cerebral root activity and inhibiton of SD activity (Fig. 3 B), which are char-

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Fig. 3 A-E. Comparison of effects of PC cell stimulation during quiescent conditions and during primary rhythms elicited by esophageal nerve stimulation (see Methods). A, B Example of results from one particular PC ceils. A During quiescent conditions, PC cell stimulation elicited a strong motor pattern with alternating activity in buccal roots (R3 and RI), phasic activity in cerebral roots (SOVN and MN), and variable activity in the SD. B During a primary rhythm (starting at left), the same stimulation (right) accelerates the pattern, produces more tonic SOVN and MN activity, and inhibits SD activity for three cycles. C, D Example from a different PC cell. A During quiescent conditions, PC cell stimulation elicited a strong motor pattern in which all the components, including the SD, were phasically active. D During a primary rhythm (left before record) the same stimulation accelerates the pattern and inhibits the SD for several cycles. E Example of an inhibitory PC cell. This cell did not elicit motor activity under quiescent conditions, but could inhibit an on-going primary rhythm (center of record)

acteristics of vomiting rhythms. More dramati- cally, stimulation of a different PC cell during quiescent conditions elicited a strong motor pattern with SD bursts occurring during each cycle (Fig. 3 C), while the same stimulation applied during a primary rhythm not only accelerated the pattern but also actively inhibited SD bursts and produced several SOVN bursts during the end of RI

538 A.D. McClellan: Diversity of cerebral ganglia neurons in Pleurobranchaea

R3 SD

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Fig. 4. PC cell activity during motor patterns elicited by esophageal nerve stimulation (see Methods). Very few cells were active during primary rhythms (left and right sections of record). During vomiting rhythms (between arrows; note inactivity in SD) about 38% of the PC cells burst in phase with RI activity

activity (Fig. 3D; note that the primary rhythm started before the beginning of the record and to the right). The latter pattern of SD and SOVN activity has previously been shown to occur only during vomiting rhythms (McCellan 1982 b). These effects were repeatable and were not the result of PC cell stimulation being applied before the occur- rence of a spontaneous episode of vomiting.

The PC cells described so far were located near the base of the tentacle nerve and were excitatory. One or two inhibitory neurons with axons in the CBC could be found anterior to this region, between the tentacle nerve and SOVN (McClellan 1980; also see Cohan 1980). Stimulation of these latter PC cells (n = 11) during quiescent conditions was usually without effect, but stimulation during an on-going primary rhythm resulted in clear inhibition of the pattern (Fig. 3 E). In different preparations the inhibition could be partial or complete and could affect different components of the pattern.

Many of the PC cells were not active during the generation of motor activity, but about 38% (12 of 32) of the cells fired bursts in phase with R1 activity during vomiting rhythms (Fig. 4, between arrows). Many of these PC cells were excitatory (82%) but did not elicit a specific type of motor pattern. These PC neurons began to fire bursts as the vomiting rhythm approached termination, but the causality of this relationship was not tested further.

Discussion

Metacerebral cells

The main finding here is that the MCGs have a relatively weak and variable effect on the motor network, and that these cells become less active or inactive during transitions to vomiting rhythms. The latter finding could be explained by the fact that the MCG is indirectly inhibited by the ventral

white cell (Davis 1977), which was recently shown to activate and fire high frequency bursts during vomiting (McClellan 1979, 1983).

In different gastropod species, presumed homologies of the MCG have been thought to control initiation (Pleurobranchaea; Gillette and Davis 1977), modulation (Limax; Prior and Gelperin 1975), and arousal (Aplysia; Weiss et al. 1978) of feeding behavior. In all these preparations the MCGs activate weak motor patterns. In contrast, the MCG cells in Helisoma elicit strong buccal rhythms which are thought to underlie feeding (Granzow and Kater 1977). Since feeding in Heli- soma is essentially a 'fixed-action pattern' reflex (Kater 1974), the command system for this behavior could be comparatively simple and consist of only the MCG cells. In other gastropods, feeding is more variable and dependent on motivational and associative factors (Mpitsos and Davis 1973; Gelperin 1975; Davis et al. 1977; Mpitsos etal. 1978), and the feeding command function might have been transferred from the MCGs to a larger, more flexible group of higher order cells, such as the PC neurons (McClellan 1980).

Paracerebral neurons

Previous results have suggested that some of the PC cells are part of a homogeneous group which activates feeding (Davis 1977), and some of these neurons are in fact active during feeding in relatively intact preparations (Gillette et al. 1978). The new results presented here suggest a somewhat more complex function for these cells: (a) PC neurons are part of a heterogenous group which elicit motor activity differing in both intensity and pattern (Figs. 2, 3 A, C), and some cells are inhibitory (Fig. 3 E). (b) About 20% of the PC cells can modify an on-going primary rhythm to a pattern that resembles vomiting motor activity (Fig. 3 D; note SD inactivity). It is interesting to note that some PC cells were previously shown to activate motor


patterns in which SOVN activity was in phase with R1 bursts (Fig. 1A, B; Gillette et al. 1978), a char- acteristic of vomiting patterns (McClellan 1982b). (c) About 38% of the PC neurons fired bursts during vomiting rhythms (Fig. 4). Unfortunately it is difficult to compare the present results with previous studies where more restrictive criteria were used for selecting cells from the PC group and a smaller part of the motor activity was recorded.

Collective operation of the paracerebral cells

Approximately 10-15 PC cells appear to reside in each cerebral hemi-ganglion (Davis 1977), and as many as seven different cells have been stimulated and recorded in single preparations. Based on the stimulation results it appears that each PC cell has a specific excitatory or inhibitory effect on the motor network (e.g. Fig. 3; PC5, PC6, and PC7 are from the same preparation). Unfortunately, it is presently difficult to group the cells into more specific classes. It is nearly impossible to identify the same PC cells in different preparations based on elicited motor activity because of moderate differences in the relative amplitudes of units which con- tribute to neural burst activity. Thus, the burst envelopes of neural activity during a given motor pattern can have different shapes (but the same phasing) in different preparations (e.g. see Fig. 10 in McClellan 1982b).

If each PC cell has a different effect on the motor network, it can be expected that these cells act in different combinations to elicit complete motor patterns (Davis 1977). Variations in the types of PC cells which are active would result in variations in motor activity and behavioral function. This mechanism would be most likely to produce adaptive variations in feeding (but see below), as some of these cells have been clearly implicated in activating this behavior (Gillette et al. 1978). A similar operation has been suggested (but not proven) for systems of ' command ' cells in crusta- ceans (Evoy and Kennedy 1967; Kennedy et al. 1967; Larimer and Kennedy 1969; Davis and Ken- nedy 1972a, b; Bowerman and Larimer 1974a, b; Larimer and Gordon 1976) and mollusks (Balaban 1979).

The buccal mass of PIeurobranchaea is used during several behaviors (see Introduction), and the differences in the motor patterns underlying these responses are only moderate or have not yet been completely determined (McClellan 1980, 1982a). Since some PC cells can activate motor activity that resembles vomiting patterns (Fig. 3 D) and some cells are active during vomiting rhythms

(Fig. 4), the possibility must be considered that some of these cells have non-command functions (e.g. coordination, termination), or are involved in activating motor functions besides feeding or possibly in addition to feeding. The PC cells are apparently not active during rejection (i.e. 'egestion') of unpalatable objects (e.g. string, rubber tubing) but some were activated by stimulation of the ventral white cells (Gillette et al. 1982), higher order neurons in the buccal ganglia which have recently been shown to activate vomiting motor patterns (McClellan 1979, 1980, 1983). These possibilities need to be tested further in semi- intact preparations, because in isolated preparations it is difficult to determine the specific conse- quences of motor activity, except for vomiting patterns.

Assuming that the PC cells act together, what factors might control the combinations of cells which are active at any one time? Sensory inputs can be expected to directly or indirectly activate various PC neurons depending on the desired func- tional outcome. Feedback from the motor network could also affect the types of cells active and their pattern of activity. The PC cells activate different motor patterns from the motor network in the buccal ganglia, and depending on the elicited pattern different buccal-cerebral interneurons are activated (Cohan 1980; Cohan and Mpitsos 1983) which then exert excitatory or inhibitory effects on the PC cells (Gillette et al. 1978). The net effect of this is a complex feedback loop between the cerebral and buccal ganglia in which the relevant 'descend- ing' and 'ascending' elements are heterogenous. A very detailed description of this feedback network will be necessary in understanding the initiation and generation of different buccal motor patterns in Pleurobranchaea.

Context of command cell stimulation

Stimulation of 20% of the excitatory PC cells during a primary rhythm can modify the on-going motor activity to resemble a vomiting pattern (Fig. 3 B, D). This result may seem at odds with the evidence that some PC cells are activated by chemosensory inputs and appear to initiate feeding (Davis 1977; Davis and Gillette 1978). However, presentation of food to chemosensory structures of Pleurobranchaea does not invariably elicit feeding, but can sometimes evoke vomiting responses, especially from dissected preparations (McClellan 1980, 1982a). Thus, it is possible that some PC cells elicit different responses, such as feeding or vomiting, depending on conditions within the too-

540 A.D. McClellan: Diversity of cerebral ganglia neurons in Pleurobranchaea

tor networks. This could be one of the mechanisms contributing to motivation and behavioral state.

Similar effects have been found in the cockroach, where stimulation of the same giant inter- neuron during different sensory conditons can elicit either walking or flight motor activity (Ritzmann et al. 1980). In general, some command neurons may not be simple ' push-buttons ' (Wiersma 1952) but could elicit different responses depending on internal conditions. This would result in greater efficiency of the neurons available for controlling multifunctional structures, such as the buccal mass.

Acknowledgements. I would especially like to thank Dr. George Mpitsos for helpful suggestions and encouragement during the course of this study. The discussions with Dr. C. Cohan are also gratefully acknowledged. I would like to thank Prof. S. Grillner, and Drs. K. Sigvardt and P. Wallen for crificising an earlier version of the paper. The author was supported by NIH grants GM 01090 and GM 07535 awarded to the Dept. of Biomed. Eng., CWRU, and the work was supported by NSF grant BNS 76-81233 awarded to Dr. G. Mpitsos, Dept. of Anatomy, CWRU.

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higher order neurons in the cerebral ganglia ofpleurobranchaea have diverse effects on buccal motor...

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