Action-inhibition hierarchies: Using a simple gastropod model to investigate serotonergic and dopaminergic control of action selection and reinforcement learning

IntroductionBasal ganglia (BG) activity plays an important role in action selection and reinforcement learning. Inputs from and to other areas of the brain are modulated by a number of neurotransmitter pathways in the BG. Disturbances in the normal function of the BG may play a role in the aetiology of psychiatric disorders such as schizophrenia and bipolar disorder.AimsDevelop a simple animal model to evaluate interactions between glutamatergic, dopaminergic, serotonergic and GABAergic neurones in the modulation of action selection and reinforcement learning.ObjectivesTo characterise the effects of changing dopaminergic and serotonergic activity on action selection and reinforcement learning in an animal model.MethodsThe food seeking / consummation (FSC) activity of the gastropod Planorbis corneus was suppressed by operant conditioning using a repeated unconditioned stimulus-punishment regime. The effects of elevated serotonin or dopamine levels (administration into cerebral, pedal and buccal ganglia), on operantly-conditioned FSC activity was assessed.ResultsOperantly-conditioned behaviour was reversed by elevated ganglia serotonin levels but snails showed no food consummation motor activity in the absence of food. In contrast, elevated ganglia dopamine levels in conditioned snails elicited food consummation motor movements in the absence of food but not orientation towards a food source.ConclusionsThe modulation of FSC activity elicited by reinforcement learning is subject to hierarchical control in gastropods. Serotoninergic activity is responsible establishing the general activity level whilst dopaminergic activity appears to play a more localised and subordinate ‘command’ role.

The suppressive excretory–secretory product of Trichobilharzia ocellata: a possible factor for determining compatibility in parasite–host interactions

Factors which may determine trematode–snail interactions were assessed in the present study. Compatibility was examined using a bacterial clearance assay to detect the modulatory effects of both compatible and incompatible trematode infections on the activity of haemocytes from Lymnaea stagnalis, during the early stages of infection. Exposure to and injection with Trichobilharzia ocellata, a compatible trematode, or the incompatible Schistosoma mansoni, resulted in modulation of haemocyte activity. However, T. ocellata activated haemocytes 1·5 h post-infection (p.i.) and then suppressed activity 24–72 h p.i. whereas with S. mansoni no suppression, only activation of haemocytes was observed throughout the test period (1·5–72 h p.i.). In previous studies, modulation of the haemocyte clearance activity by T. ocellata was found to be mediated by 2 E–S fractions, an activating fraction and a suppressing one. Investigations to assess whether the lack of suppression of haemocyte activity, observed in the S. mansoni–L. stagnalis incompatible trematode–snail interaction studied, was due to either the absence or ineffectiveness of the suppressing E–S fraction, were performed on a second incompatible combination, T. ocellata–Planorbis corneus. Using this combination it was revealed that only the activating E–S fraction had modulatory effects on P. corneus haemocytes, indicating that the suppressing E–S fraction, which actively interferes with the clearance activity of haemocytes from L. stagnalis, appears to act in a host-specific manner. In conclusion, the suppressing E–S fraction determines, at least in part, compatibility in the trematode–snail association studied. This is also probably likely in other trematode–snail combinations.

Defense reaction in the pond snail Planorbis corneus. I. Activity of the shell-moving and respiratory systems

1. In the intact pond snail Planorbis corneus, tactile or electrical stimulation of the skin evoked a biphasic general defense reaction. A weak stimulation evoked only the first phase of the reaction, represented as a fast pulling of the shell towards the head. With stronger stimulation, this phase was followed by the second phase that was comprised of three components: detachment from the substrate, slow retraction of the body into the shell, and letting out of air from the lung through the pneumostome. 2. About 70 motor neurons (MNs) of the columellar muscle have been revealed in different ganglia by means of their cobalt back-filling through the cut columellar nerve. A complicated pattern of electrical coupling was found for different groups of MNs. Excitation of individual MNs, evoked by current injection, resulted in contraction of the columellar muscle (CNS-columellar muscle preparation). The strongest contraction was evoked by the cerebral MNs; fast small contraction by the parietal MNs; and slow, long-latency contraction, by the pedal MNs. 3. In the same preparation, electrical stimulation of the cutaneous (lip) nerve evoked biphasic contraction of the columellar muscle (a first phase lasting approximately 3 s, and a second phase of up to 1 min). The temporal pattern of this response was similar to that of the defense reaction in the intact animal. A weak stimulation evoked only the first phases of the reaction, while a stronger stimulation evoked both phases. The amplitude of both the first and the second phase was graded with the strength of stimulation.(ABSTRACT TRUNCATED AT 250 WORDS)

Defense reaction in the pond snail Planorbis corneus. III. Response to input from statocysts

1. In the intact pond snail Planorbis corneus, a rapid tilt in any plane evoked a defense reaction consisting of a fast movement of the shell towards the head, shortening of the foot, inhibition of locomotion and of rhythmical feeding movements. This reaction was similar to the first phase of the general defense reaction of Planorbis to cutaneous stimulation. 2. A method has been developed for inclination of the isolated CNS in space (up to 90 degrees) and simultaneous intracellular recordings from different neurons. 3. The statocyst receptor cells (SRCs) responded both phasically and tonically to the tilt. The SRCs differ in their spatial zones of sensitivity. 4. Essential manifestations of the defense reaction to the input from statocysts could be observed in the in vitro preparation of the CNS isolated with statocysts. Both tilting of the CNS and electrical stimulation of individual SRCs elicited an excitatory response in numerous neurons from different ganglia, including motor neurons (MNs) of the columellar muscle. This response was of "all-or-none" nature, and could be evoked by electrical stimulation of any SRC. The response was followed by a long (10-20 s) period of refractoriness. 5. Activation of SRCs resulted also in excitation of the giant dopaminergic cell in the left pedal ganglion (related to the control of respiration), in inhibition of the feeding rhythm generator, and in inhibition of the pedal neurons responsible for activation of the ciliary locomotor system. 6. Combined stimulation of two inputs able to evoke a defense reaction, i.e., those from the statocyst and from cutaneous nerve, revealed a strong interdependence of their central effects.(ABSTRACT TRUNCATED AT 250 WORDS)

Defense reaction in the pond snail Planorbis corneus. II. Central pattern generator

1. In the isolated CNS of the pond snail Planorbis corneus, spontaneous bursts of activity in the motor neurons (MNs) supplying the columellar muscle were occasionally observed. The biphasic pattern of this activity, with a shorter (3-5 s) initial burst and longer (20-40 s) subsequent burst, was similar to that of the motor output during the general ("whole-body") defense reaction. In preparations consisting of the CNS isolated with the columellar muscle or with the lung, spontaneous biphasic contractions of the muscle as well as openings of the pneumostome with a temporal pattern characteristic of the defense reaction were observed. These findings demonstrated that the efferent pattern of the defense reaction in the snail is, to a large extent, produced by a special neuronal mechanism (the central pattern generator, CPG) triggered by the sensory input, rather than generated by ongoing processing of sensory input. The CPG consists of two components responsible for generation of two phases of the defense reaction. A characteristic feature of the CPG is that the magnitude of its response depends in a graded fashion on the strength of the initial stimulus. 2. In the pleural ganglia there are at least two electrically connected interneurons (DRN1s) that play an important role in generation of the first phase of the defense reaction. Processes of the DRN1s form a ring passing through all (except pedal and buccal) ganglia. The DRN1s received an excitatory input when a peripheral nerve was stimulated. They generated action potentials of long (0.2-2 s) duration. The DRN1 from the right ganglion was studied in more detail.(ABSTRACT TRUNCATED AT 250 WORDS)