Control of habituation of the withdrawal reflex by the gill ganglion in <i>Aplysia</i>

Peretz, Bertram; Møller, R. C.

doi:10.1002/neu.480050303

Cited by 29 publications

(13 citation statements)

References 28 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For example, inhibitory junction potentials in gill musculature (14) and the suppressive influence of the PVG on the peripheral pathway (15) may contribute. Also, the branchial (gill) ganglion, which is important in gill habituation to direct gill stimulation (21,22) may contribute. Responses of the isolated siphon to direct siphon stimulation also readily habituate (23)(24)(25).…”

Section: Discussionmentioning

confidence: 99%

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

The gill withdrawal reflex of Aplysia has been used as a model for studying the neuronal mechanisms of habituation, a behavioral plasticity. We have assessed the contribution of neuromuscular facilitation, an elementary synaptic plasticity, during habituation of the reflex by recording gill muscle potentials, which we show are caused by excitatory junctional potentials. These potentials show systematic frequency-dependent changes in amplitude. The gill withdrawal evoked by central motor neuron firing during each habituation trial is determined by facilitation of the excitatory junctional potentials during the trial and the facilitated state of the initial excitatory junctional potential in a trial, determined by neuron activity prior to the trial. The neuromuscular junctions, therefore, act like a frequency-dependent amplifier of central motor activity. They are fully responsive to the dynamic changes of motor neuron firing that occurs during habituation and especially after dishabituation.The neural correlates of habituation have been extensively studied in three invertebrate preparations, the crayfish (Procambaxrus) (1-3), the locust (Schistocerca) (4), and the sea hare (Apiysia). Habituation, the decrement of a behavioral response with repeated stimulation and its restoration or dishabituation by a novel stimulus, can be studied in these preparations at the level of synaptic communication between neurons. In these animals, and possibly in vertebrates (5), homosynaptic depression at central neuronal synapses has been identified as a mechanism of habituation (1-4, 6, 7).In Aplysia the reflex withdrawal of the gill evoked by siphon stimulation has been used as a model for the study of habituation (7-9). Several central motor neurons participate in this reflex, and studies of motor neuron L7 have shown that it receives excitatory postsynaptic potential (EPSP) input from a cluster of central sensory neurons (10-12). These EPSPs decrease in amplitude with successive stimuli and therefore, as a consequence of a decrease in the number of quanta of transmitter released (13) at the sensory-motor chemical synapses, homosynaptic depression has been proposed as the mechanism of habituation of the reflex (7, 9). The train of action potentials evoked by synaptic input to neuron L7 during behavioral habituation and dishabituation has been shown (9) but the firing of other major motor neurons (LDG1 and LDG2) has not. The firing of L7 decreases slowly during behavioral habituation of the gill and recovers slowly after dishabituation (9). If habituation is caused solely by synaptic depression at sensory-motor synapses (9, 13), the firing of the motor neurons should parallel the evoked gill withdrawal because these neurons synapse directly on gill muscles and are reported to produce temporally stable nondecrementing gill withdrawal (10, 14). However, it was shown that the neuron-gill muscle synapses showed pronounced facilitation (14).We examined the possibility that changes in the efficacy of gill neuromuscular junction...

show abstract

Section: Discussionmentioning

confidence: 99%

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…As mentioned earlier, at least one major class of mechanoreceptors has so far eluded detection; the identities of sensory receptors mediating very low threshold tactile responses involving various head and mantle regions are presently unknown (Rosen et al, 1991;Frost et al, 1997;Hickie et al, 1997;Walters and Cohen, 1997). In addition, the touch receptors mediating local withdrawal reflexes in Aplysia Peretz and Moller, 1974;Peretz et al, 1976) have never been identified. Indeed, Sakharov and Salanki (1980), examining the effects of pharmacological depletion of dopamine in the land snail Helix, concluded that catecholamines probably play significant roles in withdrawal reflexes and other behaviours elicited by tactile stimulation.…”

Section: Functions Of Peripheral Neuronesmentioning

confidence: 92%

“…For instance, despite over 30 years of extensive study, it is now apparent that a major class of mechanosensory neurones involved in the gill withdrawal reflex has escaped identification (Frost et al, 1997;Hickie et al, 1997;Walters and Cohen, 1997), and only a portion of the many sensory neurones that probably contribute to other behaviours such as the appetitive and consummatory aspects of feeding is known (Preston and Lee, 1973;Audesirk, 1975;Emery and Audesirk, 1978;Rosen et al, 1979;Xin et al, 1995). Even more broadly, the entire peripheral nervous system, although long known to be both extensive and complex (Bulloch and Horridge, 1965), is largely unexplored (but see Peretz and Moller, 1974;Bailey et al, 1976;Xin et al, 1995).…”

mentioning

confidence: 98%

Catecholamine‐containing cells in the central nervous system and periphery of Aplysia californica

Croll

2001

J of Comparative Neurology

View full text Add to dashboard Cite

Previous studies have suggested the presence of numerous catecholamine-containing cells in both the central ganglia and peripheral tissues of Aplysia, but they often offered conflicting or incomplete accounts of numbers, locations, and morphologies. The current study combines aldehyde-induced histofluorescence and tyrosine hydroxylase-like immunoreactivity together with confocal microscopy to provide details of these cells. Approximately 35-50 neurones in the cerebral ganglia, 4-8 neurones in the pedal ganglia, 5 neurones in the buccal ganglia, and numerous small fibres in various nerve trunks exhibited both immunoreactivity and aldehyde-induced fluorescence. Approximately 20 cells in the pedal ganglia and 4 cells in the buccal ganglia exhibited only immunoreactivity whereas 15-20 neurons in the cerebral ganglia exhibited only aldehyde-induced fluorescence. No somata in the pleural or abdominal ganglia exhibited aldehyde-induced fluorescence or immunoreactivity. Both aldehyde-induced histofluorescence and immunoreactivity also labelled what appeared to be two classes of catecholamine-containing cells in the gill, siphon, oesophagus, rhinophore, tentacle, and reproductive organs. The more numerous, but smaller cells had subepithelial somata and processes penetrating the overlying body wall, thus suggesting a sensory function. Another class of neurones had larger somata, often located more deeply within the tissue, and occasionally appeared to be multipolar. Processes from these various peripheral cells appeared to comprise the major component of afferent fibres and to form an extensive peripheral plexus, often associated with various muscles. The morphologies of the peripheral cells thus suggest involvement in both local and centrally mediated reflexes and responses, but additional studies must test such hypothesised functions and determine the sensory modalities that the cells mediate.

show abstract

“…Other tests of the plexus such as stimulation of the branchial and ctcnidial nerves (Fig. 1), which causes well coordinated gill movement (Peretz and Moiler, 1974) also showed the plexus to be as developed as in older animals.…”

Section: Behavioral Di//erence8 Between Young and Older Animalsmentioning

confidence: 95%

Age-dependent CNS control of the habituating gill withdrawal reflex and of correlated activity in identified neurons inAplysia

Peretz

Lukowiak

1975

J. Comp. Physiol.

Self Cite

View full text Add to dashboard Cite

Summary. The parieto-visceral ganglion (PVG) control of the gill withdrawal reflex to tactile stimulation of the gill is absent in young animals, weighing 25 g or less. In older animals, weighing 160 g or more, the PVG control causes suppression of the reflex amplitude and a faster rate of habituation. 1) In young Aplysia the PVG did not suppress the reflex amplitude nor did it accelerate the rate of habituation (Fig. 2). The gill neural plexus, through which presumably, PVG control of the reflex is mediated, is as competent in young as in older animals to mediate habituation (Fig. 2).2) PVG control was not evoked by increasing the intensity of the tactile stimulus 12 fold, from 0.15 g to 1.8 g, to the gill; in older animals the extent of control was dependent on stimulus intensity (Fig. 3).3) In young animals the 0.15 g stimulus evoked spiking in L~, a gill motor neuron, and it evoked only an EPSP in L~ in older Aplysia (Figs. 4, 5). The decrement of evoked activity in L~ from both groups of animals was correlated with habituation of the reflex (Fig. 8).4) Induced spiking of L~, in young and older Aplysia, resulted in dishabituation of the gill reflex (Fig. 8). These results and those in (3) show that the pathways between the gill and the PVG are functional in young animals. 5) No differences were found in membrane properties of L~ from young and older animals; L~'s were only differentiated by cell size (Table 1, Figs. 6, 7). 6) In contrast R2, which is not involved in the reflex, was responsive to the weaker gill stimuli only in young animals (Figs. 4, 5). Re's greater responsiveness is attributed to small cell size which accounts for greater input resistance (Table 1, Fig. 7).7) The absence of control of the gill withdrawal reflex and the greater synaptic efficacy in L~ to gill stimulation, we suggest, results from incompletely developed inhibitory mechanisms in the PVG of young animals (Fig. 9).

show abstract

Control of habituation of the withdrawal reflex by the gill ganglion in Aplysia

Cited by 29 publications

References 28 publications

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Catecholamine‐containing cells in the central nervous system and periphery of Aplysia californica

Age-dependent CNS control of the habituating gill withdrawal reflex and of correlated activity in identified neurons inAplysia

Contact Info

Product

Resources

About