Transfer of Habituation Shows an Interaction Between Neuronal Circuits of the Gill Withdrawal Reflex in Aplysia Californica

1982 ◽  
Vol 96 (1) ◽  
pp. 107-124
Author(s):  
JEFF GOLDBERG ◽  
KEN LUKOWIAK

The gill withdrawal reflex (GWR) and its subsequent habituation can be evoked by tactile stimulation of the siphon or gill when the CNS is either intact or removed. It has been suggested that the neural circuits that mediate the GWR evoked at these two loci are parallel and independent. We provide three lines of evidence which show that these circuits interact and, therefore, comprise a single integrated system. Firtly, siphon and gill stimulation evoked similar excitatory responses in the central gill motor neurones. Secondly, the GWR habituated by repetitive stimulation at one locus was dishabituated by stimulation of the other locus. Thirdly, transfer of habituation occurred. Although the transfer was seen neurally at the level of central gill motor neurones, transfer of habituation also occurred after the CNS was removed. Therefore, the neuronal circuits mediating the reflexes evoked at the siphon and gill interact within both the CNS and PNS. The PNS is largely responsible for mediating this gill behaviour that is based on such interactions, while the CNS provides suppressive and facilitatory plasticity to these responses to enable Aplysia to better adapt to a changing environment.

1990 ◽  
Vol 68 (11) ◽  
pp. 1407-1413
Author(s):  
David Cawthorpe ◽  
Ken Lukowiak

Acetylcholine (ACh) dissolved in seawater and perfused through the isolated gill of the Aplysia californica produced suppression of the gill withdrawal reflex (GWR) evoked by tactile stimulation of the gill. This suppression was reversible upon washout and was blocked by co-perfusion of curare and α-bungarotoxin. Co-perfusion of atropine did not block the suppression of the GWR produced by ACh. We concluded that the suppressive effects produced by perfusion of ACh through the gill occur as a result of the action of ACh at the nicotinic-like receptors. The role of ACh suppression in the mediation of gill reflex behaviours is discussed.Key words: Aplysia, gill withdrawal reflex, suppression, acetylcholine.


1978 ◽  
Vol 56 (6) ◽  
pp. 1079-1082 ◽  
Author(s):  
Ken Lukowiak

The gill withdrawal reflex evoked by tactile stimulation of the siphon in Aplysia habituates with repeated presentation of the stimulus. This adaptive behaviour is mediated by the integrated activity of the central (CNS) and peripheral (PNS) nervous systems. The PNS mediates the basic reflex and its habituation while the CNS exerts both suppressive and facilitatory control over the PNS. This results in greater adaptability of the reflex behaviours. In young Aplysia the CNS control is absent and this is due to the incomplete development of pathways in the CNS. In an attempt to identify the pathway an attempt was made to manipulate the CNS's suppressive influence by agents which antagonize putative neurotransmitters. The application of picrotoxin-containing seawater over the CNS removed the CNS's suppressive influence but not its facilitatory influence. Thus the reflex amplitude was increased, the reflex latency decreased, and repeated stimulation did not result in habituation. This effect of picrotoxin was completely reversible. It is thus proposed that γ-aminobutyric acid, a putative neurotransmitter, plays an important rote in the mediation of the CNS's suppressive influence.


1978 ◽  
Vol 41 (2) ◽  
pp. 418-431 ◽  
Author(s):  
J. H. Byrne ◽  
V. F. Castellucci ◽  
E. R. Kandel

1. To evaluate the contribution which mechanoreceptor sensory neurons make to the defensive gill-withdrawal reflex we developed an isolated reflex preparation. We then reduced this isolated reflex to a microcircuit (consisting of a single sensory cell and single motor cell) so as to causally relate the contribution of individual cells to the expression and plastic properties of the behavior. 2. Mechanoreceptor neurons make significant contributions to the amplitude and duration of the complex PSP in the motor neurons. A single spike in a sensory neuron produces an EPSP in the motor neuron which accounts for 7-36% of the complex EPSP produced by weak tactile stimulation of the skin. 3. More than 50% of the synaptic input to the gill motor neurons appears to be monosynaptic. Perfusing the ganglion with solutions of high divalent cations reduced the motor neurons' complex PSP by only 40%. 4. The population response of the mechanoreceptors to a point stimulus can be simulated by repetitively firing a single sensory neuron. Firing a single sensory cell discharges the motor neuron and produces a gill contraction similar to that produced by a natural stimulus. 5. Mechanoreceptors make monosynaptic connections onto gill motor neurons which decrement with repeated stimulation paralleling the decrement of the complex PSP to punctate tactile stimulation of the skin. 6. The results indicate that the known neural elements may quantitatively account for most of the expression of the behavior and its short-term habituation.


1983 ◽  
Vol 61 (7) ◽  
pp. 743-748 ◽  
Author(s):  
Ken Lukowiak ◽  
Lee Freedman

In Aplysia, the central nervous system and peripheral nervous system interact and form an integrated system that mediates adaptive gill withdrawal reflex behaviours evoked by tactile stimulation of the siphon. The central nervous system (CNS) exerts suppressive and facilitatory control over the peripheral nervous system (PNS) in the mediation of these behaviours. We found that the CNS's suppressive control over the PNS was increased significantly in animals engaged in sexual activity as either a male or female. In control animals, the evoked gill withdrawal reflex met a minimal response amplitide criterion, while in sexually active animals the reflex did not meet this criterion. At the neuronal level, the increased CNS suppressive control was manifested as a decrease in excitatory input to the central gill motor neurons.


1981 ◽  
Vol 91 (1) ◽  
pp. 145-164
Author(s):  
R. D. HAWKINS ◽  
J. BRUNER

1. The activity of the opener excitor and inhibitor motor neurones was recorded during habituation and dishabituation of the defensive claw opening response in partially restrained crayfish (Astacus sp.). 2. Claw opening evoked by brief tactile stimulation of the thorax undergoes habituation if the stimulation is repeated at 30 s or 1 min intervals. This habituation is accompanied by a progressive decrease in evoked excitor activity, while the activity of the inhibitor remains unchanged. 3. The habituated claw opening response can be dishabituated by tactile stimulation of the claw or head, or by visual stimulation. Dishabituation is accompanied by both an increase in evoked excitor activity and a decrease in evoked inhibitor activity. 4. Dishabituation is also accompanied by potentiation of claw opening: that is, the same number of excitor and inhibitor spikes produce greater claw opening following dishabituating stimulation. 5. The potentiation of claw opening following dishabituation is due in part to post-tetanic potentiation (PTP) at the excitor neuromuscular junction. PTP was demonstrated with physiological parameters of stimulation in isolated claw preparations, and is of sufficient magnitude and duration to account for the observed potentiation. 6. These results contradict the conclusion from an earlier study (see Schöne, 1961) that habituation of the claw opening response is due to an increase in inhibitor activity. They also provide new evidence for a role in dishabituation of both disinhibition and PTP.


1996 ◽  
Vol 199 (3) ◽  
pp. 683-691 ◽  
Author(s):  
K Lukowiak ◽  
E Ringseis ◽  
G Spencer ◽  
W Wildering ◽  
N Syed

In this study, we operantly conditioned the aerial respiratory behaviour of the freshwater snail Lymnaea stagnalis. Aerial respiration in Lymnaea stagnalis is accomplished by the spontaneous opening and closing of its respiratory orifice, the pneumostome, at the water surface. Weak tactile stimulation of the pneumostome area, when the pneumostome is open, evoked only the pneumostome closure response, which is one aspect of the escape-withdrawal reflex. Pneumostome stimulation resulted in its closure and the termination of aerial respiratory activity. A contingent tactile stimulation paradigm was used to operantly condition the animals. Stimulation of the pneumostome whenever the animal attempted to breathe resulted in significantly fewer attempts to open the pneumostome as training progressed. The latency of the first breath (subsequent to stimulation), the number of breaths and the total breathing time were measured before and after each training period. Significant, quantifiable changes in these behavioural parameters were observed only in the operant conditioning group animals. Control animals receiving tactile stimulation to their pneumostome not contingent upon pneumostome opening movements (yoked controls) or those that were physically prevented from surfacing to breathe (hypoxic controls), did not exhibit significant changes in these behavioural parameters. Our data provide the first direct evidence for operant conditioning of respiration in any animal.


1982 ◽  
Vol 47 (5) ◽  
pp. 885-908 ◽  
Author(s):  
R. Gillette ◽  
M. P. Kovac ◽  
W. J. Davis

1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally symmetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns pme subset pf [MCs. the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PNCs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the "bite"). No other behavorial effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excited by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bit. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific "command" neurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. In isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PNC-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8...


1989 ◽  
Vol 62 (6) ◽  
pp. 1225-1236 ◽  
Author(s):  
S. M. Gurahian ◽  
S. H. Chandler ◽  
L. J. Goldberg

1. The effects of repetitive stimulation of the nucleus pontis caudalis and nucleus gigantocellularis (PnC-Gi) of the reticular formation on jaw opener and closer motoneurons were examined. The PnC-Gi was stimulated at 75 Hz at current intensities less than 90 microA. 2. Rhythmically occurring, long-duration, depolarizing membrane potentials in jaw opener motoneurons [excitatory masticatory drive potential (E-MDP)] and long-duration hyperpolarizing membrane potentials [inhibitory masticatory drive potentials (I-MDP)] in jaw closer motoneurons were evoked by 40-Hz repetitive masticatory cortex stimulation. These potentials were completely suppressed by PnC-Gi stimulation. PnC-Gi stimulation also suppressed the short-duration, stimulus-locked depolarizations [excitatory postsynaptic potentials (EPSPs)] in jaw opener motoneurons and short-duration, stimulus-locked hyperpolarizations [inhibitory postsynaptic potentials (IPSPs)] in jaw closer motoneurons, evoked by the same repetitive cortical stimulation. 3. Short pulse train (3 pulses; 500 Hz) stimulation of the masticatory area of the cortex in the absence of rhythmical jaw movements activated the short-latency paucisynaptic corticotrigeminal pathways and evoked short-duration EPSPs and IPSPs in jaw opener and closer motoneurons, respectively. The same PnC-Gi stimulation that completely suppressed rhythmical MDPs, and stimulus-locked PSPs evoked by repetitive stimulation to the masticatory area of the cortex, produced an average reduction in PSP amplitude of 22 and 17% in jaw closer and opener motoneurons, respectively. 4. PnC-Gi stimulation produced minimal effects on the amplitude of the antidromic digastric field potential or on the intracellularly recorded antidromic digastric action potential. Moreover, PnC-Gi stimulation had little effect on jaw opener or jaw closer motoneuron membrane resting potentials in the absence of rhythmical jaw movements (RJMs). PnC-Gi stimulation produced variable effects on conductance pulses elicited in jaw opener and closer motoneurons in the absence of RJMs. 5. These results indicate that the powerful suppression of cortically evoked MDPs in opener and closer motoneurons during PnC-Gi stimulation is most likely not a result of postsynaptic inhibition of trigeminal motoneurons. It is proposed that this suppression is a result of suppression of activity in neurons responsible for masticatory rhythm generation.


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