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Department of Physiology and Biophysics, Mt. Sinai School of Medicine, New York, New York 10029
Submitted 9 May 2004; accepted in final form 26 May 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). Under physiological conditions, however, CPGs often receive sensory input so that output is adjusted to compensate for changes in the periphery. In fact, in some cases, sensory neurons are considered to be an integral part of a CPG (e.g., Pearson et al. 1983). In many systems, therefore, the generation of behaviorally relevant motor programs cannot be understood unless processes that integrate peripheral and central activity are characterized. A number of studies that have provided insights into how this type of integration occurs have utilized experimentally advantageous invertebrate preparations. We are studying sensorimotor integration during feeding behavior in one such preparation, the marine mollusc Aplysia.
A number of studies have shown that rhythmic activity can be triggered in the feeding circuitry of Aplysia in preparations in which connections between the nervous system and peripheral structures are severed (Church and Lloyd 1994; Hurwitz et al. 2003; Jing and Weiss 2001, 2002; Jing et al. 1999, 2003; Morgan et al. 2000, 2002; Proekt and Weiss 2003; Rosen et al. 1991; Sanchez and Kirk 2000, 2001; Susswein et al. 1996). These results indicate that there is a feeding CPG. Under physiological conditions, however, feeding in Aplysia shows a great deal of plasticity that is likely to be induced by afferent input. For example, when Aplysia are in the general vicinity of food, they will generate ingestive responses, bites, even if they are not able to grasp food (Kupfermann 1974). Bites consist of two antagonistic sets of radula movements; radula opening and protraction is followed by radula closing and retraction. When an animal bites, the radula opens and protracts vigorously, but it does not fully retract, and activity in radula closing/retraction motor neurons is relatively brief (Weiss et al. 1986). If bites are successful and the radula does close on food, bites are converted to bite-swallows, i.e., radula closing and retraction is enhanced and prolonged so that food will be pulled through the buccal cavity and deposited in the esophagus (Cropper et al. 1990; Kupfermann 1974; Weiss et al. 1986). Thus bite to bite-swallow conversions are presumably triggered by afferent activity, e.g., by afferent input from the site of food contact (the radula).
Afferent input that triggers bite to bite-swallow conversions is likely to be provided, in part, by radula mechanoafferents (RMs) (Miller et al. 1994), such as the identified neuron B21 (Rosen et al. 2000b). RMs are relatively low threshold mechanoafferents that have receptive fields on the biting surface of the radula (Miller et al. 1994; Rosen et al. 2000b). These neurons are activated whenever anything touches the radula; therefore they will be activated when food contact occurs and/or when the radula closes on food. Other sensory neurons that are likely to be activated when bites are converted to bite swallows are proprioceptors that are activated when retraction movements are induced, i.e., retraction proprioceptors (RPs) (Evans and Cropper 1998). RPs are activated when the resistance to backward rotation is increased (as it can be when food is pulled into the buccal cavity) (Evans and Cropper 1998). The largest and best-characterized RP is a neuron originally described as an interneuron, B51 (Plummer and Kirk 1990).
RMs and RPs are located in the buccal ganglion (Evans and Cropper 1998; Miller et al. 1994; Plummer and Kirk 1990; Rosen et al. 2000b). Previous studies have characterized synaptic connections of the identified neurons B21 and B51 and have shown that both cells are electrically coupled to, or make excitatory connections with, radula closing and retraction interneurons and motor neurons (Evans and Cropper 1998; Klein et al. 2000; Plummer and Kirk 1990; Rosen et al. 2000b). Both neurons are therefore depolarized via central input during retraction (Borovikov et al. 2000; Evans et al. 2003; Rosen et al. 2000a, b). During biting-like motor programs, this depolarization is often subthreshold or only triggers low-frequency activity. When food is ingested, however, retraction activity in B21 and B51 would be increased (via peripheral activation). In this study, we show that increases in activity in B21 and B51 will change the activity of the feeding circuitry during biting-like motor programs in a manner consistent with the bite to bite-swallow conversion.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Experiments were performed on 100- to 150-g Aplysia californica (Marinus, CA) maintained in 14–16°C holding tanks. Prior to dissection, animals were anesthetized by injection of isotonic MgCl2 (50% of body weight). The cerebral and buccal ganglia were removed, and all nerves were severed that connect the buccal ganglion with the buccal mass and esophagus. The paired radula nerves were cut close to where they disappear into the buccal mass to leave a sufficient length for extracellular recording. Additionally the I2 nerve was initially left intact. Its innervation of the I2 muscle was subsequently severed with the aid of a dissecting microscope. Ganglia were placed in a Sylgard-coated dish and pinned (the buccal ganglion rostral side up, the cerebral ganglion ventral side up). The buccal and cerebral ganglia were pharmacologically isolated by surrounding the cerebral ganglion with a circle of silicone vacuum grease (Dow Corning, Midland, MI) and by gently placing a polyethylene ring on top of the layer of grease.
Electrophysiology
Neurons were impaled with single barreled glass microelectrodes filled with 2 M potassium acetate, beveled to an impedance of 6–12 M
. Two microelectrodes were connected to an AxoClamp 2B (Axon Instruments, Burlingame, CA), and two to Getting Model 5A amplifiers (Getting Instruments, Iowa City, IA). Two extracellular suction electrodes were connected to Grass Model P511 amplifiers (Grass Medical Instruments, Quincy, MA). Outputs from the amplifiers led to a PCM recording adapter model 3000A (Vetron Technology) connected to a Sony VCR for archival data storage. Output from the Vetter PCM was split so that it passed to an oscilloscope (Tektronix Model 5111), a thermal printer (AstroMed MT9500), and an ITC-16 A-D converter (Instrutech, Long Island, NY) connected to a Macintosh G4 computer (Apple Computer, Cupertino, CA). Data were acquired and analyzed using Axograph v4.0 software (Axon Instruments). When stimulator-driven current injection was needed, it was provided by either TTL pulses from a Grass S48 stimulator (for simple pulse trains) triggering current via the "step activate" port on the AxoClamp, or in the case of more complex protocols, by output programmed into the AxoGraph program, and sent via the ITC-16 interface into the "ext command" port of the AxoClamp.
Solutions
Normal artificial seawater (ASW) was composed of (in mM) 460 NaCl, 10 KCl, 11 CaCl2, 55 MgCl2, and 10 HEPES (pH 7.6). All salts were from Sigma (St. Louis, MO). Modified ASW (2:1 ASW) (Trudeau and Castellucci 1992), for suppressing polysynaptic activity, contained twice the normal concentration of Mg2+ and 1.25 times the normal concentration of CaCl2.
Generation and modification of motor programs
Biting-like motor programs were generated by replacing the ASW bathing the cerebral ganglion with a solution of 3 mM carbachol in ASW (Susswein et al. 1996). Protraction was monitored by extracellular recordings from the I2 nerve, which contains the axons of the motor neurons that innervate a muscle that produces protraction movements, the I2 muscle (Hurwitz et al. 1996) (i.e., the I2 nerve innervates the I2 muscle). Retraction was monitored by extracellular recordings from the RN, in which high-frequency activity immediately following protraction is indicative of ingestive-like activity (Morton and Chiel 1993a). Intracellular recordings were obtained from sensory neurons and one to three additional previously characterized interneurons or motor neurons.
In experiments in which effects of increases in afferent activity were studied, sensory neurons were intracellularly depolarized with DC to achieve a firing rate of 12–16 Hz. Physiological firing patterns of sensory neurons during bite to bite-swallow conversions have not been described, but these types of increases in afferent activity are observed when sensory neurons are peripherally activated in semi-intact preparations (Borovikov et al. 2000; Evans and Cropper 1998). Depolarization was initiated at the start of high-frequency activity in B8 or the RN and was continued until just after retraction terminated to insure that the termination of retraction was not simply due to the cessation of current injection.
Presentation of data
Typically, the effect of an afferent neuron on the motor program was shown by comparing three cycles of activity: the cycle before the sensory neuron was stimulated (labeled before), the cycle in which the sensory neuron was stimulated (labeled during), and the cycle following sensory neuron stimulation (labeled after). Duration reflects the duration of depolarization from baseline during retraction. For neurons that were strongly activated during retraction, duration reflects the duration of high-frequency firing. Frequency reflects the number of spikes divided by the duration of spike burst during retraction. Significance was determined using repeated-measure ANOVA with Fischer's PLSD posthoc analysis comparing the three cycles of activity. All values are given as mean ± SE.
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RESULTS |
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). Figure 1, A and B, shows two examples of carbachol-generated motor programs, demonstrating the timing of activity of several buccal neurons. The ingestive motor program consists of three components. Synchronous activity in the opening/protraction neurons occurs first, seen in Fig. 1A as activity in B61 and the I2 nerve, which carries axons of motor neurons (including B61) innervating the major protractor muscle, the I2 muscle (i.e., the I2 nerve innervates the I2 muscle).
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; Orekhova et al. 2001), and B64, a retraction interneuron (Hurwitz and Susswein 1996). Radula mechanoafferent B21 and motor neuron B15 (implicated in radula closing and retraction; Cohen et al. 1978; Cropper et al. 1990; Orekhova et al. 2001) also receive depolarizing input during this time, but are generally not strongly activated. The protraction motor neuron B61, on the other hand, is hyperpolarized during closing/retraction. Also seen in Fig. 1 is activity in the RN. Large amplitude extracellular activity in this nerve is due to activity in radula closer neurons. The fact that, in the carbachol-generated motor programs, radula closer activity is phase locked to retractor activity provides good evidence that these programs are indeed ingestive-like.
A third component of activity can be seen in Fig. 1 as well. It appears as a gap between the end of closing/retraction and the beginning of the subsequent opening/protraction. There is little to no bursting activity in the I2 or RN nerves at this time, but as shown in Fig. 1B, there is high-frequency activity in neuron B52. B52 makes inhibitory connections with the closing/retraction circuitry but it does not make excitatory connections with the opening/protraction circuitry, and it does not appear to have any motor output of its own (Baxter et al. 1997; Evans et al. 1999; Plummer and Kirk 1990). The B52 activity that follows retraction therefore represents a time in which closing/retraction activity is inhibited, but opening/protraction movements have not yet been initiated. Radula movements during this third component of the motor program have not been completely characterized (but see DISCUSSION). We refer to this as the postretraction component of the motor program.
Stimulation of B21
Bites are converted to bite-swallows when food contacts the radula and the radula closes on food during closing/retraction (Weiss et al. 1986). Presumably this stimulation of the radula surface will activate radula mechanoafferents, including B21. In these experiments, B21 was therefore phasically activated during retraction. In initial experiments, we sought to determine whether increases in afferent activity could produce changes in the activity of characterized motor neurons that produce radula closing or retraction [Fig. 2, 1)]. Activation of B21 did in fact produce a significant increase in the duration of activity of the radula closer motor neuron B8 (before, 3.35 ± 0.27; during, 7.11 ± 0.59; after, 3.41 ± 0.32 s; Fig. 3A) and in the radula closer/retractor B15 (before, 3.47 ± 0.50; during, 7.91 ± 1.15; after, 4.03 ± 0.70 s; Fig. 3B). Additionally, B21 stimulation produced a significant increase in the firing frequency of these two motor neurons (B8—before, 16.70 ± 1.66; during, 19.40 ± 1.72; after, 15.70 ± 1.66 Hz: B15—before, 1.27 ± 0.95; during, 4.23 ± 1.11, after, 1.66 ± 0.67 Hz; Fig. 3, A and B).
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) retraction interneuron, B64. We observed a significant increase in the duration of B64 activity (before, 3.10 ± 4.20; during, 7.03 ± 1.44; after, 3.44 ± 0.33 s; Fig. 4). Moreover, the activity in B64 remains phase-locked to the high-frequency activity in the RN, indicating that the alteration of the motor program by B21 is a coordinated, multilevel effect.
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) and 2) in the onset of spiking activity in the interneuron B52 (Plummer and Kirk 1990) [Fig. 2, 3)]. In both cases, we found a significant increase in the duration of closing/retraction hyperpolarization as a result of B21 activity (B61—before, 3.23 ± 1.0; during, 5.76 ± 1.50; after, 3.30 ± 1.11 s: B52—before, 2.50 ± 0.30; during, 4.83 ± 0.35; after, 2.74 ± 0.23 s; Fig. 5). In other words, the onset of the postretraction component of the motor program and opening/protraction were both delayed so that the duration of the postretraction component was preserved and there was no overlap between closing/retraction and opening/protraction.
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). This circuitry includes both retraction interneurons (e.g., B64) and retraction motor neurons (e.g., B15). Previous studies have shown that interneuron stimulation alters parametric features of motor programs (e.g., Dembrow et al. 2003; Hurwitz et al. 1997; Jing and Weiss 2001, 2002; Jing et al. 2003; Teyke et al. 1993). Since electrical coupling exists between B21 and motor neurons, it was possible that the prolongation of closing/retraction was due to the secondary depolarization in coupled cells rather than the activation of B21. To determine whether directly activating motor neurons could recreate this effect, we performed experiments in which we injected current into the accessory radula closer motor neuron B15. Current injection into B15 had no significant effect (Fig. 7,A vs. B). Closing/retraction duration was not prolonged, and moreover, despite the continued injection of current into B15, there was no increase in the duration of B15 activity. Rather, B15 firing ceased due to a barrage of inhibitory postsynaptic potentials (IPSPs) at the end of closing/retraction.
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A second type of sensory neuron that presumably plays a role in the bite to bite-swallow conversion is the cell B51 (Evans and Cropper 1998). In a previous study, which was conducted in a semi-intact preparation, we showed that DC current injection into B51 alters radula movements during carbachol-induced motor programs, i.e., when B51 is continuously depolarized, radula retraction movements are enhanced (Evans and Cropper 1998). Previous work did not, however, study the effect of phase specific activation of B51. Additionally, effects of B51 stimulation on the feeding circuitry were not specifically described.
We injected current into B51 neurons during closing/retraction and found a significant increase in the firing frequency and duration of activity of radula closer motor neuron B8 (B8 duration—before, 3.13 ± 0.36; during, 6.77 ± 0.49; after, 3.04 ± 0.27 s: B8 firing frequency—before, 8.59 ± 1.63; during, 14.80 ± 1.10; after, 8.35 ± 1.40 Hz; Fig. 8A). Additionally we observed a significant increase in the duration of depolarization in radula retractor motor neuron B15 (before, 3.13 ± 0.71; during, 4.85 ± 0.67; after, 3.68 ± 0.68 s; Fig. 8B) and a significant increase in the duration of activity of retraction interneuron B64 (before, 3.01 ± 0.56 s; during, 4.77 ± 1.10; after, 3.23 ± 0.91 s; Fig. 9). Thus B51 stimulation prolonged and enhanced radula closing/retraction.
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). It was therefore possible that the increased duration of inhibition seen when B51 was active would lead to an increased rate of B52 firing immediately after B51 was active. This functionality fits with the proposed role of B52 as a neuron that terminates retraction (Baxter et al. 1997; Nargeot et al. 2002). However, the B52 firing frequency was relatively unchanged when B51 was fired despite the longer duration of inhibition. Relationship between B21 and B51
B21 and B51 exhibit bi-directional electrical coupling (Fig. 11). Thus it is possible that when current is injected into B51 during rhythmic activity, B21 could also be activated and could mediate the observed changes in motor programs. In a similar vein, when current is injected into B21, B51 could be activated. To determine whether either or both of these possibilities occur, we performed experiments in which we induced changes in motor programs and recorded from both cells. When current was injected into B51, B21 was not activated (Fig. 12). Activity in B21 is therefore not essential for B51-induced increases in retraction duration.
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), this produced a decrease in the duration of retraction. Our data indicate therefore that B51 is not essential for B21-induced alterations in motor programs.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Evans et al. 2003; Miller et al. 1994; Rosen et al. 2000a, b). Additionally, previous studies characterized central synaptic connections of B21 and B51 and showed that both cells make direct excitatory connections with the radula closing/retraction circuitry (Klein et al. 2000; Plummer and Kirk 1990; Rosen et al. 2000a, b). One purpose of this study was to determine whether changes in afferent activity are transmitted to the feeding circuitry during biting-like motor programs and whether these changes are consistent with the bite to bite-swallow conversion. Determining whether B21's known connections would in fact be able to alter ongoing motor programs was a crucial step in understanding B21's capabilities given that studies have shown that synaptic pathways can be heterosynaptically inhibited by other neurons of the neural network (e.g., Blitz and Nusbaum 1997; Chiel et al. 1988; DiCaprio 1999; Grillner and Wallen 1985; Nusbaum et al. 1997; Segev 1990; Storozhuk and Castellucci 1999). More specifically, Rosen et al. (2000a) have shown that activity of other neurons can significantly reduce B21's output.
The effects of B21 and B51 were determined using carbachol-generated motor programs. Analysis of these motor programs provided insights about the fundamental nature of the neural network underlying ingestive motor programs. For instance, we noted that neuron B52 fired at the highest frequency during a period in the motor program in which the network appeared otherwise relatively quiescent (labeled as the postretraction component in Fig. 1). A study by Evans and Cropper (1998) found that, immediately following the retraction phase, there was a short burst of activity in the radula opener motor neuron B48, but this burst did not persist for the entire duration of activity in B52. Hence, although the Aplysia ingestive motor program is generally regarded as biphasic (e.g., Church and Lloyd 1994; Evans et al. 1999; Morgan 1999), our results indicate that a triphasic description of the motor program is also possible (see Murphy 2001 for a recent review).
It is possible to reconcile the triphasic motor program with the apparently biphasic ingestive behavior. Evans et al. (1999) recorded from B52 while monitoring radula movements. Examination of the simultaneous B52 recording and radula movement record shown in Fig. 13 of Evans and Cropper (1998) actually shows a two-phase trajectory from the peak of retraction to the subsequent peak of protraction. Immediately following the peak of retraction, one sees a shallow protraction trajectory, indicating a relatively slower moving forward of the radula. After this, there is an abrupt, steep trajectory protraction, indicating a forceful, swift protraction movement. Weiss et al. (1986) theorized, based on measurements of hydrostatic pressure in the artery that supplies the buccal mass, that after an active retraction beyond the midrange, or "rest" position, the radula exhibits a passive "return protraction" followed by an active protraction. This may explain why there is still movement of the radula, although the motor program does not indicate motor neuron activity. Thus the active protraction is likely to be the result of the protraction motor neuron activity, while the time, in which B52 is firing, may be the shallow trajectory period during which the passive "return protraction" occurs.
When we induced activity in sensory neurons, we found that that there were significant changes in motor programs. For example, the duration of activity in the closing/retraction circuitry was prolonged, and the subsequent activation of the opening/protraction circuitry was delayed. Additionally, the firing frequency of some closing/retraction neurons was significantly increased. Interestingly, firing frequency was most dramatically changed in neurons such as the ARC motor neuron B15 that are recruited when bites are converted to bite-swallows in intact animals (Cropper et al. 1990). Thus we found that increases in afferent activity were transmitted to the feeding circuitry and showed that motor programs were altered in a manner that is similar to what is observed in intact animals when bites are converted to bite-swallows.
We showed that changes in feeding motor programs can be induced via activation of a single sensory neuron, i.e., a single B21 or a single B51. This result is somewhat unexpected. B21 and B51 are both members of clusters of cells with similar response properties (Evans and Cropper 1998; Miller et al. 1994; Rosen et al. 2000b). In theory, changes in motor programs could require simultaneous activation of many cells. It is interesting that this does not appear to be true in this case. It should be noted, however, that in this study we were not specifically mimicking bite-swallow patterns of activation of sensory neurons. Currently this is not possible since these patterns have not been characterized. In this study, therefore, sensory neurons were stimulated at frequencies that data suggest are reasonable. It is possible therefore that we are overestimating (or underestimating) single cell effects on activity during physiologically induced motor programs. Nevertheless our results indicate that it is unlikely that simultaneous activation of whole clusters of cells is essential for bite to bite-swallow conversions.
We showed that both B21 and B51 can alter motor programs. When current was injected into B51, B21 was generally not recruited. In contrast, when current was injected into B21, B51 was recruited in most, but not all, cases. This suggests that three types of afferent induced changes in motor programs might be possible: a change triggered by B51 alone, a change triggered by B21 alone, and a change triggered by B21 that then recruits B51. During a bite to bite-swallow conversion, it would seem unlikely that B51 would be peripherally activated without activation of B21. B21 is a low-threshold RM that is activated whenever the biting surface of the radula is touched (Rosen et al. 2000b). When food is ingested, it obviously contacts the radula biting surface. Thus it would seem unlikely that bite to bite-swallow conversions would be triggered by B51 alone. Instead it is more likely that they are triggered either by B21 alone or by both B21 and B51.
Changes in motor programs induced by B21 and B51 together differ from those triggered by B21 alone in that the increase in the duration of radula closing/retraction is greater when both B21 and B51 are activated. In general, an increase in the duration of activity in a feeding neuromuscular system will generate an increase in the amplitude of the evoked movement (i.e., feeding muscles are generally nonspiking and contraction amplitude is determined by the total number of spikes within a given burst of activity; e.g., see Cohen et al. 1978). Recruitment of B51 therefore presumably increases retraction movements. It is therefore possible that in some cases bite-swallow conversions can be triggered via activation of B21 alone. This may occur when a small piece of free-floating seaweed is ingested that can be readily pulled into the buccal cavity. In contrast, when a larger piece of food is ingested or when food that is attached to a substrate is ingested, the increased resistance during retraction may ensure recruitment of B51. B51 recruitment may in turn produce necessary enhancements in retraction movements. Furthermore, B21 causes B8 to fire longer and at a higher frequency. Firing of B8 produces centripetal activity in B51 (Evans and Cropper 1998). Thus B21 firing is even more likely to produce activation of B51 in an intact behaving animal.
In the isolated nervous system, we showed that, when B51 is recruited by B21, the two sensory neurons are for the most part not co-active. Spiking is immediately triggered in B21, but it is not immediately triggered in B51. When B51 does finally spike, B21 receives inhibitory input and spiking ceases. Thus in the isolated nervous system, B21 activity predominates early in retraction, whereas B51 activity predominates later in retraction (Fig. 14). With the periphery present, afferent activation could obviously occur in a different manner, e.g., B51 could be strongly peripherally activated early in retraction. Interestingly, however, we would not expect this to the case given what is currently known about feeding movements and the mechanisms that peripherally activate B21 and B51. Thus radula movements and the activity of the feeding circuitry are slightly out of synch (i.e., neural activity precedes movement) (Evans and Cropper 1998). When food is ingested, it will, therefore, presumably contact the radula at peak protraction, which will occur as activity in the retraction circuitry is initiated. Thus B21 will presumably be peripherally activated at the beginning of the retraction phase of the motor program. In contrast, B51 will not be peripherally activated until retraction has occurred, at least to some extent. This will occur later during the retraction phase of the motor program. Thus central and peripheral mechanisms are likely to work together to create a sequential pattern of afferent activation during bite to bite-swallow conversions. Functionally, this pattern of activity may create a situation in which B21 (and other RMs) primarily trigger bite to bite-swallow conversions. In contrast, B51 may predominantly insure that the magnitude of the evoked movement is appropriate for the food ingested.
In conclusion, a goal of our current research is to utilize the experimentally advantageous features of the Aplysia feeding system to study sensorimotor integration during a rhythmic motor program. These results (taken together with previous work) establish B21 and B51 as physiologically characterized afferents that can be used to study direct effects of afferent activity on pattern generation. With the possible exception of B4/5 (Fiore and Geppetti 1981; Jing and Weiss 2001) and B52 neurons (Evans et al. 1999; Nargeot et al. 2002), other Aplysia neurons that can be used for these studies have not yet been identified.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. C. Cropper, Dept. Physiology/Biophysics, Box 1218, Mt. Sinai Medical School, One Gustave L. Levy Place, New York, NY 10029 (E-mail: elizabeth.cropper{at}mssm.edu).
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