Modulation of fictive feeding by dopamine and serotonin in aplysia.

The buccal ganglia of Aplysia contain a central pattern generator (CPG) that mediates rhythmic movements of the buccal apparatus during feeding. Activity in this CPG is believed to be regulated, in part, by extrinsic serotonergic inputs and by an intrinsic and extrinsic system of putative dopaminergic cells. The present study investigated the roles of dopamine (DA) and serotonin (5-HT) in regulating feeding movements of the buccal apparatus and properties of the underlying neural circuitry. Perfusing a semi-intact head preparation with DA (50 microM) or the metabolic precursor of catecholamines (L-3-4-dihydroxyphenylalanine, DOPA, 250 microM) induced feeding-like movements of the jaws and radula/odontophore. These DA-induced movements were similar to bites in intact animals. Perfusing with 5-HT (5 microM) also induced feeding-like movements, but the 5-HT-induced movements were similar to swallows. In preparations of isolated buccal ganglia, buccal motor programs (BMPs) that represented at least two different aspects of fictive feeding (i.e., ingestion and rejection) could be recorded. Bath application of DA (50 microM) increased the frequency of BMPs, in part, by increasing the number of ingestion-like BMPs. Bath application of 5-HT (5 microM) did not significantly increase the frequency of BMPs nor did it significantly increase the proportion of ingestion-like BMPs being expressed. Many of the cells and synaptic connections within the CPG appeared to be modulated by DA or 5-HT. For example, bath application of DA decreased the excitability of cells B4/5 and B34, which in turn may have contributed to the DA-induced increase in ingestion-like BMPs. In summary, bite-like movements were induced by DA in the semi-intact preparation, and neural correlates of these DA-induced effects were manifest as an increase in ingestion-like BMPs in the isolated ganglia. Swallow-like movements were induced by 5-HT in the semi-intact preparation. Neural correlates of these 5-HT-induced effects were not evident in isolated buccal ganglia, however.

Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia.

Catecholamines are believed to play an important role in regulating the properties and functional organization of the neural circuitry mediating consummatory feeding behaviors in Aplysia. In the present study, we morphologically and electrophysiologically identified a pair of catecholaminergic interneurons, referred to as B65, in the buccal ganglia. Their processes innervate both the ipsi- and contralateral neuropil, and separate branches of B65 appeared to innervate the somata of both ipsi- and contralateral B4/5 neurons. B65 exhibited patterned burst(s) of activity during spontaneous cycles of fictive feeding. Patterned activity in B65 also was elicited by stimulation of the radula nerve, by depolarization of the pattern initiating neurons B31/32 or B63, and by bath application of -3,4-dihydroxyphenylalanine (DOPA). B65 appeared to be a member of the protraction group of neurons. Action potentials in B65 elicited fast one-for-one excitatory postsynaptic potentials (EPSPs) in neurons B4/5, B8A/B, B31/32, B63, and B64. In turn, B31/32 and B63 excited B65 and B64 inhibited B65. Some of the synaptic connections of B65 were plastic. For example, the fast EPSPs elicited in B4/5 and B64 decremented, whereas those in B31/32 andB8A/B facilitated. In addition to fast EPSPs, B65 elicited slow postsynaptic potentials in some of its follower cells. Depolarization of B65 elicited cycles of patterned activity indicative of fictive feeding in buccal neurons, including B65 itself. During series of B65-induced patterns, the properties of the buccal motor programs appeared to change. In particular, the activity of radula closure motor neurons B8A/B, which initially coincided mainly with the protraction phase of a cycle, gradually extended to overlap mostly with the retraction phase. This observation suggests that prolonged activity in B65 may play a role in transitioning from rejection-like to ingestion-like fictive feeding. The phase shift of the activity of B8A/B appears due, at least in part, to a decrease in activity of B4/5, and thus a reduction in inhibition from B4/5 onto B8A/B, during the retraction phase. The functional properties and synaptic connections of B65 suggest that it may play an important role in determining features of patterned neural activity in the buccal ganglia.

The frog brainstem preparation as a model for studying the central control of breathing in tetrapods

Our frog brainstem preparation revealed mechanisms for the central control of breathing that are in many ways similar to those of mammals. Thus, the basic control mechanisms for air-breathing appear to have been present in the Devonian common ancestors of frogs and mammals and may be common to all lung-breathing vertebrates. Location: The in vitro frog brainstem, including motor nuclei of cranial nerves V to X, maintains frequency and ratio of fictive buccal oscillations to fictive lung inflation episodes comparable with that of the living animal. In this preparation, transaction caudal to V abolishes spontaneous discharge in X but slow, spontaneous discharge in V may remain. Independent central pattern generation is present in the left and right half-brainstems. Chemosensitivity: The frequency of fictive lung inflation increases with decrease in pH within the physiological range. Response to glutamate: Biphasic response, consisting of a pause, followed by a dramatic increase in the frequency of fictive inspirations and positive baseline deflection, followed, in turn, by slow return of the baseline to the control level with frequency remaining above control as long as glutamate is applied. Local application reveals glutamate-sensitive sites in the ventral reticular formation. Response to substance P and physalaemin: Similar to glutamate but the frequency of fictive inspirations decreases below control values. Response to strychnine: The normal temporal sequence in firing of motor neurons of cranial nerves is disrupted and all nerves are synchronously active. The firing sequence of respiratory neurons is consistent with a grouping possibly homologous to the mammalian inspiratory, post-inspiratory and expiratory phases.

The frog brainstem preparation as a model for studying the central control of breathing in tetrapods.

Our frog brainstem preparation revealed mechanisms for the central control of breathing that are in many ways similar to those of mammals. Thus, the basic control mechanisms for air-breathing appear to have been present in the Devonian common ancestors of frogs and mammals and may be common to all lung-breathing vertebrates. LOCATION: The in vitro frog brainstem, including motor nuclei of cranial nerves V to X, maintains frequency and ratio of fictive buccal oscillations to fictive lung inflation episodes comparable with that of the living animal. In this preparation, transection caudal to V abolishes spontaneous discharge in X but slow, spontaneous discharge in V may remain. Independent central pattern generation is present in the left and right half-brainstems. CHEMOSENSITIVITY: The frequency of fictive lung inflations increases with decrease in pH within the physiological range. RESPONSE TO GLUTAMATE: Biphasic response, consisting of a pause, followed by a dramatic increase in the frequency of fictive inspirations and positive baseline deflection, followed, in turn, by slow return of the baseline to the control level with frequency remaining above control as long as glutamate is applied. Local application reveals glutamate-sensitive sites in the ventral reticular formation. RESPONSE TO SUBSTANCE P AND PHYSALAEMIN: Similar to glutamate but the frequency of fictive inspirations decreases below control values. RESPONSE TO STRYCHNINE: The normal temporal sequence in firing of motor neurons of cranial nerves is disrupted and all nerves are synchronously active. The firing sequence of respiratory neurons is consistent with a grouping possibly homologous to the mammalian inspiratory, post-inspiratory and expiratory phases.