Klaudiusz R. Weiss

Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs

The properties of the giant cerebral serotonin-containing neurons of the opisthobranch mollusc Aplysia californica were studied and were compared to the existing data on the giant serotonin-containing neurons (metacerebral cells) of pulmonate mulluscs. Among the properties examined were: axonal distribution, synaptic input and output, pharmacological responses, biophysical characteristics, and plasticity. With only minor exceptions, the properties of the serotonin-containing neurons of Aplysia and of pulmonate molluscs were remarkably similar, and it was concluded that these identified neurons are true homologues. The establishment of the homology of the metacerebral cells of Aplysia to the metacerebral cells of pulmonate molluscs extends the known distribution of these neurons to a second major subclass (Opisthobranchiata) of molluscs. Since pulmonate and opisthobranch molluscs differ substantially in behavioral and anatomical features, the study of the metacerebral cells of these two groups may promote the understanding of the evolutionary adaptation of the nervous system to different environmental pressures.

The effects of food arousal on the latency of biting inAplysia

SummaryExposure ofAplysia to food stimuli initiates a process leading to a state of food arousal. One aspect of this process is expressed in a progressive reduction in latency of successive biting responses. The time needed for food stimulation to produce a state of arousal (measured by a minimal latency) is affected by the satiation level of the animal, and by the strength of the food stimulus presented. Specifically, the rise of the arousal state is slowed in partially satiated animals, and in animals presented with weak food stimuli. When aroused animals are allowed a period of rest without food stimulation a decay of arousal occurs, as reflected in a rise in latency.Arousal state decays more rapidly in partially satiated animals than in non-fed animals. Effects of satiation upon arousal were mimicked by feeding animals with non-nutritive bulk, thereby demonstrating that these effects are due, at least in part, to the bulk stimuli provided by food consumed during a meal. The interaction between effects of the arousal state and satiation may help explain how feeding inAplysia is patterned into discrete meals.

Peptidergic co-transmission in Aplysia: Functional implications for rhythmic behaviors

Despite their ubiquitous presence in the central and peripheral nervous systems, the behavioral functions of peptide co-transmitters remain to be elucidated. The marine molluscAplysia, whose simple nervous system facilitates the study of the neural basis of behavior, was used to investigate the role of peptidergic co-transmission in feeding behavior. Several novel modulatory neuropeptides were purified, and localized to identified cholinergic motorneurons. Physiological and biochemical studies demonstrated that these peptides are released when the motorneourons fire at frequencies that occur during normal behavior, and that the peptides modify the relationship between muscle contraction amplitude and relaxation rate so as to maintain optimal motor output when the intensity and frequency of feeding behavior change.

Activity of an identified serotonergic neuron in free moving Aplysia correlates with behavioral arousal

Extracellular recordings of the metacerebral cell (MCC), a serotonergic neuron in Aplysia, were obtained in free moving, undrugged animals. MCC activity was evoked by exposure to food. Arousal level was manipulated by satiating the animals or exposing them to a noxious stimulus. We found that the amount of evoked MCC activity correlated with the level of arousal of the animal.

Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry ofAplysia

We have identified a buccal neuron (B20) that exhibits dopamine-like histofluorescence and that can drive a rhythmic motor program of the feeding motor circuitry of Aplysia. The cell fires vigorously during episodes of patterned buccal activity that occur spontaneously, or during buccal programs elicited by stimulation of identified cerebral command-like neurons for feeding motor programs. Preventing B20 from firing, or firing B20 at inappropriate times, can modify the program driven by the cerebral feeding command-like neuron CBI-2. When B20 is activated by means of constant depolarizing current it discharges in phasic bursts, and evokes a sustained coordinated rhythmic buccal motor program. The program incorporates numerous buccal and cerebral neurons associated with aspects of feeding responses. The B20-driven program can be reversibly blocked by the dopamine-antagonist ergonovine, suggesting that dopamine may be causally involved in the generation of the program. Although firing of B20 evokes phasic activity in cerebral command-like neurons, the presence of the cerebral ganglion is not necessary for B20 to drive the program. The data are consistent with the notion that dopaminergic neuron B20 is an element within the central pattern generator for motor programs associated with feeding.

Release of Peptide Cotransmitters in Aplysia: Regulation and Functional Implications

To gain insights into the physiological role of cotransmission, we measured peptide release from cell B15, a motorneuron that utilizes ACh as its primary transmitter but also contains putative peptide cotransmitters, the small cardioactive peptides (SCPs) and the buccalins (BUCs). All stimulation parameters used were in the range in which B15 fires in freely moving animals. We stimulated neuron B15 in bursts and systematically varied the interburst interval, the intraburst frequency, and burst duration. Both peptides were preferentially released when B15 was stimulated at higher intra- or interburst frequencies or with longer burst durations. Across stimulation patterns, the amount of peptide released depended on the mean frequency of stimulation and was independent of the specific pattern of stimulation. The parameters of stimulation that produce a larger release of peptides correspond to those that evoke larger contractions. Large and frequent contractions are likely to fuse or summate, thus disrupting the rhythmic behavior mediated by the muscle innervated by motorneuron B15. Because the combined effect of the SCPs and BUCs is to accelerate the relaxation and shorten the duration of muscle contractions, these peptides reduce the probability of the disruptive fusion or summation of muscle contractions. Because these cotransmitters regulate an aspect of muscle contractions that is not controlled by acetylcholine (ACh), the primary transmitter of B15, we suggest that peptides and ACh form parallel but functionally distinct lines of transmission at the neuromuscular junction. Both types of transmission may be necessary to ensure that behavior remains efficient over a wide range of conditions.

The Construction of Movement with Behavior-Specific and Behavior-Independent Modules

Growing evidence suggests that different forms of complex motor acts are constructed through flexible combinations of a small number of modules in interneuronal networks. It remains to be established, however, whether a module simply controls groups of muscles and functions as a computational unit for use in multiple behaviors (behavior independent) or whether a module controls multiple salient features that define one behavior and is used primarily for that behavior (behavior specific). We used the Aplysia feeding motor network to examine the two proposals by studying the functions of identifiable interneurons. We identified three types of motor programs that resemble three types of behaviors that Aplysia produce: biting, swallowing, and rejection. Two ingestive programs (biting, swallowing) are defined by two movement parameters of the feeding apparatus (the radula): one is the same in both programs (phasing of radula closure motoneurons relative to radula protraction-retraction), whereas the other parameter (protraction duration) is different in the two programs. In each program, these two parameters were specified together by an individual neuron, but the neurons in each were different (B40 for biting, B30 for swallowing). These findings support the existence of behavior-specific modules. Furthermore, neuron B51 was found to mediate a phase that can be flexibly added on to both ingestive and egestive-rejection programs, suggesting that B51 may be a behavior-independent module. The functional interpretation of the role played by these modules is supported by the patterns of synaptic connectivity that they make. Thus, both behavior-specific and behavior-independent modules are used to construct complex behaviors.

Interneuronal Basis of the Generation of Related but Distinct Motor Programs in Aplysia: Implications for Current Neuronal Models of Vertebrate Intralimb Coordination

Coordination of two sets of movements, protraction–retraction versus opening–closing, of the feeding apparatus (the radula) in ingestive and egestive motor programs of Aplysiaresembles vertebrate intralimb coordination in that the relative timing of the two sets of movements differs in the two motor programs. In both ingestion and egestion, radula protraction and retraction alternate, whereas radula closure shifts its phase relative to protraction–retraction. In egestion, the radula closes in protraction; in ingestion, the radula closes in retraction. In both ingestive and egestive motor programs elicited by the command-like neuron, cerebral-buccal interneuron-2 (CBI-2), the protraction and retraction movements are mediated by the same sets of controller interneurons. In contrast, radula closure is mediated by two controller interneurons, B20 and B40, that are preferentially active in egestion and ingestion, respectively. In egestion, B20, active in protraction, drives closure motorneuron B8 in protraction, whereas in ingestion, B40, also active in protraction, uses a functionally novel mechanism, fast inhibition and slow excitation, to drive B8 in retraction. Our findings are summarized in a neural model that permits a conceptual comparison of our model with two previous hypothetical models of intralimb coordination in spinal circuits that were proposed by Grillner (1981,1985) and Berkowitz and Stein (1994). Although our model supports the existence of separate controllers for different movements as in theGrillner (1981, 1985) model; in terms of basic mechanisms, our model is similar to the Berkowitz and Stein (1994) model because the closure movement is mediated by separate controllers in different programs, and thus both models can be classified as recruitment models.

Differential firing patterns of the peptide-containing cholinergic motor neurons B15 and B16 during feeding behavior inAplysia

During egestive responses neuron B16 fires at 20 Hz, while neuron B15 is not active. During ingestive responses B16 fires for 0.5-1.0 s at 15-20 Hz, then B15 and B16 fire together, with B15 firing at 7.5-12 Hz. The duration of activity during ingestive responses depends on consumption of food: when food is not consumed, bursts are shorter (e.g. 2 vs 4 s). This study establishes a basis for investigating the role of peripheral neuromodulation under physiologically relevant conditions.

Appetitive feeding behavior of Aplysia: behavioral and neural analysis of directed head turning.

The appetitive phase of feeding behavior in Aplysia consists of a behavioral sequence in which the quiescent animal starts to locomote and then assumes a characteristic feeding posture. In this position, head-turning responses can be elicited by a localized food stimulus (seaweed) delivered to the lips or tentacles. In response to brief (open loop) stimulation with seaweed, the animal turns toward the stimulus but greatly overshoots the target. However, the angular velocity and the final turning angle are a function of the eccentricity of the stimulus, progressively increasing with greater eccentricities. In a food-aroused animal, a brief tactile stimulus evokes turning and biting responses similar to those triggered by seaweed, which provides both tactile and chemical stimulation. Upon repeated tactile stimulation, however, the response magnitude decrements rapidly, whereas the magnitude remains high when turning responses are repeatedly elicited by food stimuli. A purely chemical stimulus sometimes can elicit a turning response, but chemical stimuli alone are much less efficacious than tactile stimuli alone. When the stimulus is maintained in a stationary position (closed loop), the animal turns until its mouth is oriented over the food. A turning response to a lateral stimulus can be reduced by an immediately following medial stimulus. To explain the above findings, we propose a form of response substitution, in which the response to the first, lateral stimulus is substituted by a weaker response to a more medial stimulus. No turning response is evoked when the animal is stimulated while performing spontaneous or evoked bites, though biting per se does not interrupt ongoing turning movements. In animals with lesions of the cerebral- buccal connectives, a food stimulus on the mouth is also followed by a reduction of the capacity of stimuli to elicit turning responses. In these lesioned animals, the food stimulus appears to elicit a bite command, though the biting behavior itself does not occur. Thus, it appears that the bite-related gating of stimuli is of cerebral origin, rather than due to the generation of the buccal motor program. The force necessary to power the turning movements was calculated from the trajectories of the movements. The results indicate that a power phase during the first half of the duration of the total movement is sufficient to generate a turn. The power phase can be followed by a brief gliding phase, and finally the movement appears to be actively terminated.(ABSTRACT TRUNCATED AT 400 WORDS)