CNS control over gill reflex behaviors in Aplysia: Satiation causes an increase in the suppressive control in older but not young animals

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Abstract
The CNS and PNS interact and form an integrated system which mediates adaptive gill withdrawal reflex behaviors evoked by tactile stimulation of the siphon. The CNS exerts suppressive and facilitatory control over the PNS in the mediation of these behaviors. It was found that in Aplysia the CNS's suppressive control over the PNS was significantly greater than in nonsatiated control animals. In the controls, the evoked gill reflex met a mimimal response amplitude criterion with the CNS and PNS present, while in the satiated group the reflex did not meet this criterion. In the control group, the reflex amplitude and the subsequent habituation were the same following removal of the CNS, while in satiated animals the reflex amplitude was larger and the rate of habituation slower with only the PNS intact. Satiation had no effect on young Aplysia since CNS control was not yet operable. It is thus of prime importance to take the “state” of the preparation into consideration in the analysis of the neural mechanisms that underlie adaptive gill reflex behaviors. The gill withdrawal reflex and its subsequent habituation evoked by repeated tactile stimulation of the siphon in Aplysia has been studied extensively in an attempt to gain an understanding of the neuronal mechanisms that underlie adaptive behavior (Jacklet and Lukowiak, 1975; Kandel, 1976). It has been found that the central (CNS) and peripheral (PNS) nervous systems in Aplysia interact and form an integrated system which normally mediates both the reflex and its subsequent habituation (Peretz, Jacklet, and Lukowiak, 1976; Lukowiak and Peretz, 1977). Further, it was found that in the integrated system the CNS exerted both suppressive and facilitatory control over the PNS in the mediation of gill reflex behaviors (Lukowiak, 1977a). Removal of only the CNS's suppressive control over the PNS, while leaving intact its facilitatory influence, resulted in a significant reduction in reflex latency, a significant increase in reflex amplitude, and a reflex that is resistant to habituation with repeated stimulation (Lukowiak, 1977a). In addition, it was found that an identifiable neuron, L9, could modulate the ability of the reflex to habituate (Lukowiak, 1979a). With induced tonic low‐level activity in Ls the reflex evoked by repeated siphon stimulation did not habituate even though the synaptic decremental process which occurs in gill motor neurons such as L7 and accompanies gill reflex habituation (Castellucci et al., 1970) continued to occur. The neurons in abdominal ganglion, which by their activity exert control over the PNS and thus the reflex, have not yet been identified but it is known that these same neutrons apparently exert control over the synaptic input received by gill motor neurons such as L7 from the central sensory neurons (Byrne, Castellucci, and Kandel, 1974) as a result of siphon stimulation (Peretz and Lukowiak, 1975; Lukowiak and Peretz, 1980). Thus, the relative balance between the CNS's suppressive and facilitatory control will in large measure determine the overall responsiveness of the reflex and its ability to habituate. It is not, however, clear whether the CNS suppressive and facilitatory control over gill reflex behaviors evoked by siphon stimulation is altered as a result of changes in the animal's other behaviors or changes in its immediate environment. What is already known is that the CNS control is absent in young animals (Lukowiak, 1979b). In a related species, Pleurobranchaea, it has been shown that there is a behavioral hierarchy in that certain unrelated behaviors take precedence over other behaviors (Kovac and Davis, 1977; Davis and Gillette, 1978; Davis, 1979). Thus, it may be that in Aplysia changes in the relative balance between the suppressive and facilitatory CNS control over the PNS occur as result of behavioral or environmental factors. For instance, any factor that would increase CNS suppressive control would result in a smaller gill withdrawal reflex and a faster rate of habituation or a factor that increases the facilitatory control would result in a larger reflex and a tendency not to habituate. One aim of these sets of experiments was to determine how satiation affects CNS control of adaptive gill reflex behaviors and the associated synaptic input to central gill motor neurons evoked by tactile stimulation of the siphon. The other aim was to clarify the inconsistency between results previously reported (Lukowiak, 1977a) and the recent report of Carew et al. (1979). They reported that if a minimal response amplitude criterion was imposed on a preparation, that is, the evoked gill withdrawal reflex amplitude must be at least 35% of the amplitude of the large spontaneous gill respiratory movement (SGM), then the CNS mediated 90–95% of the gill reflex amplitude. Previously, it was reported (Lukowiak, 1977a) that there was no significant difference in the reflex amplitude with and without the CNS present when the reflex was evoked by the “tapper” (see Methods section). Thus, in the present study, an examination was made in preparations that met the minimal response amplitude criterion for whether removal of the CNS had a significant effect on the gill reflex amplitude. It is now reported that in adult animals that have had continuous access to food and are satiated, the CNS suppressive control over the PNS is significantly greater than in animals that have not been exposed to food. The increased suppressive CNS control is observed as a significantly smaller reflex amplitude, a faster rate of habituation, and a decrease in excitatory synaptic input to central gill motor neuron L7. Additionally, it was found that in young Aplysia, continual access to food had no effect on the reflex, its habituation, and the synaptic input to gill motor neuron L7. As concerns the second aim of this article, I found that the gill withdrawal reflex evoked by siphon stimulation with the “tapper” in all control group preparations met the minimal response criterion, and in these preparations there was no significant difference in the reflex amplitude with and without the CNS present. In the experimental group (satiated animals) none of the preparations met the minimal response criteria with the CNS intact; but, following removal of the CNS, the evoked reflex was significantly larger, in fact it met the minimal response criterion. Thus, in the control group (i.e., unsatiated animals) the results obtained do not agree with those obtained by Carew et al. (1979). In the control group preparations there was no difference in reflex amplitude or in habituation of the reflex before and after removal of the abdominal ganglion; this is in agreement with earlier results (Lukowiak, 1977a, 1979b). In experimental group preparations (i.e., satiated animals) it was found that the results agreed quantitatively with the Carew et al. (1979) report. That is, the amplitude of the reflex was larger following removal of the abdominal ganglion. However, this was due to the fact that satiation led to greater CNS suppressive control over the PNS. Thus, when the CNS control was removed, the reflex amplitude increased and the rate of habituation slowed.