Irving Kupfermann

Neuronal Correlates of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia

We have examinived the nieural correlates of habittuatiotn atid dishabitiuation of tlhe gill-withdrwal reflex in Aplysia. We obtained intracelllular recordings from identified gill motor neurons in the abdominal ganglionz of a semi-intact preparation of Aplysia wlhile we simultaneously recorded behavior responises of the gill. Habituation and dishabituation were not due to peripheral changes in either the sensory receptors or the gill musculature butt were caused by changes in the amplitlude of the excitatory synaptic potentials produced at the gill motor neurons.

Feeding behavior in Aplysia: a simple system for the study of motivation

Feeding behavior in the marine molluse Aplysia californica consists of a complex sequence of appetitive and consummatory behaviors. The consummatory behavior involves a biting response, mediated by the buccal musculature. The buccal musculature is also involved in swallowing and rejection responses. Constant stimulation with food results in regularly occurring, repetitive biting responses. The ratio of the median initial latency to interresponse times of repetitive biting was determined in order to test the predictions made by several alternative neuronal models of rhythmic biting. The data were consistent with a model in which biting is driven by a rhythmic oscillatory that is inactive until initiated by food stimuli. Control of feeding in Aplysia was examined by studying the effects on the biting response of a number of factors that affect feeding in higher organisms. A large meal was found to produce a state of satiation, characterized by a lack of locomotion and failure to exhibit biting responses to food stimuli. In a nonsatiated animal, brief contact with food was followed by an “arousal” response consisting of orienting movements, and a reduced latency to exhibit biting responses to a second food stimulus. Animals also showed a reduced latency for biting responses during the light period of a daily light-dark cycle. The advantageous properties of the nervous system of Aplysia have been utilized to study relatively simple behaviors. The present results suggest that Aplysia can be used to study more complex behaviors under extensive motivational control. Several observations in the literature indicate that many of the findings of feeding in Aplysia are also likely to apply to other gastropod molluscs with nervous systems that are advantageous for neurophysiological analysis.

Habituation and Dishabituation of the GM-Withdrawal Reflex in Aplysia

A behavioral reflex mediated by identified motor neurons in the abdominal ganglion of Aplysia undergoes two simple forms of shortterm modification. When the gill-with-drawal reflex was repeatedly evoked by a tactile stimulus to the siphon or mantle shelf, the amplitude of the response showed marked decrement (habituation). After a period of rest the response showed spontaneous recovery. The amplitude of a habituated response was facilitated by the presentation of a strong tactile stimulus to another part of the animal (dishabituation). Many characteristics of habituation and dishabituation in Aplysia are similar to those in vertebrates.

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.

Neuronal Controls of a Behavioral Response Mediated by the Abdominal Ganglion of Aplysia

Tactile stimulation of the siphon and mantle shelf in Aplysia causes a characteristic withdrawal response of the external organs of the mantle cavity. A similar response also occurs spontaneously. Both responses are mediated by the abdominal ganglion and therefore provide an opportunity for correlating cellular functioning and behavior in a relatively simple and well-studied neuronal system. The withdrawal responses are controlled by five identified motor cells which receive two types of synaptic inputs. One set of excitatory connections, activated by tactile stimulation of the siphon and mantle shelf, mediates the defensive withdrawal reflex. A second set of connections is activated by a spontaneous burst of activity in a group of closely coupled interneurons which are excitatory to some of the motor cells and inhibitory to the others. This second set of connections mediates the spontaneous withdrawal response. These two inputs can therefore switch the same population of motor cells from a simple reflex to a more complex, internally organized response.

Behavior patterns of Aplysia californica in its natural environment

Aplysia are normally exposed to great variations of water temperature, wave shock, food abundance, and duration of exposure to air. The behavior of A . in the field was very similar to that of A . in the laboratory, although there were some differences. The differences, however, appeared to be largely accounted for by the greater environmental variety in the field compared to laboratory environments. Systematic observations were made on four classes of behavior: feeding behavior, sexual behavior, locomotion, and defensive behavior. Feeding was the most frequent behavior observed. Although animals fed during a large proportion of the day, there were periods during which they would not eat, either after a normal meal, or after a meal which was fed to them by the experimenter. Animals showed definite food preferences, but large animals appeared to exhibit relatively less selectivity. Sexual behavior (copulation and egg laying) was observed to occur at a special location where the same animals remained over a period of a week or longer. During exposure to air in the intertidal zone, animals were inactive, but otherwise they locomoted over a distance of 10 m or more per day. Animals were typically found to be aggregated into groups. Defensive withdrawal occurred very infrequently and spontaneous inking behavior was never observed.

Dissociation of the appetitive and consummatory phases of feeding behavior in Aplysia: a lesion study

In order to study the relationship between the initial appetitive phases of feeding and later consummatory phases, lesions were made of specific ganglia and interganglionic connections in Aplysia californica. Animals were tested for up to three weeks following surgery so that the effects of the anesthesia and trauma were minimized. We found that the appetitive and consummatory responses are differentially affected by various lesions. Removing the buccal ganglia or severing both cerebral-buccal connectives eliminated the consummatory (biting) phase of feeding. On the other hand, severing the cerebral-pedal pleural connectives eliminated the main appetitive phase (head waving) of feeding. Control lesions of the abdominal ganglion or of single connectives of bilateral pairs did not differentially eliminate appetitive and consummatory responses. The data suggest that although the appetitive and consummatory phases of feeding occur sequentially, the motor expression of the two phases can be dissociated, and are not necessarily causally linked.

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.

The stimulus control of biting inAplysia

SummaryA number of different parameters of the biting response ofAplysia californica were examined while varying either the strength of excitatory stimuli that elicit biting, or the strength of inhibitory stimuli that suppress biting and produce satiation. Response amplitude, response latency and the interresponse interval of repetitive responses were the parameters investigated. In individual animals as well as in the mean data, all parameters of the biting response were found to be affected in a graded manner when the concentration of seaweed extract was varied, and when animals were fed to different levels of satiation. Feeding animals with non-nutritive bulk produced graded effects similar to those seen when animals were fed with seaweed. These results indicate that the biting response is modulated in a graded manner by external stimuli which elicit the response, as well as by internal stimuli which produce satiation.

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.