Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
COMM UNIGATION
Dopamine modulation of gill reflex behavior in Aplysia PETER RUBENAND KENLUKOWIAK Division of PBlysiologicud Sciences, Utziversity of Calgury, Calgary, Alta., Canada T2N IN4
Received November 6 , 1978
RUBEN, P., and LUKOWIAK, K. 1979. Dopamine modulation of gill reflex behavior in Aplysia Can. J. Physiol. Pharmacol. 57, 329-332. We have studied the effects of dopamine on the gill withdrawal reflex evoked by tactile siphon stimulation in the margine mollusc Aplysia. Physiological concentratio~ssof dopamine (diluted in seawater) were perfused through the gill during siphon stimulation series. The amplitude of the reflex was potentiated by dopamine and habituation of the reflex was prevented. This occurred with no change in the activity evoked in central motor neurons. These results lead us to conclude that the dopaniinergic motor neuron L9is modulating habituation in the periphery and that the central nervous system facilitatory control of the peripheral nervous system may act via a dopaminergic pathway.
Introduction The gill withdrawal and its subsequent habituation evoked by repeated tactile stilnulation of the siohon has been shown to be mediated bv the integrated activity of the CNS and PNS ( ~ u k d w i a k and Peretz 1977). In the integrated system, the CNS exerts both facilitatorv and sumressive control over PNS-mediated adaptiGe gill rekkx behaviors (Per& et al. 1976; ~ ~ k 1977 ~ 1. ~ The i ~ balance k between the facilitatory and suppressive iilfiuences determines the reflex amplitude, latency, and rate of habituation. How and where the CNS exerts its control is not yet k~lown.Recently, Lukowiak ( 1978n, 1978b) has found that induced low level tonic activity in the gill motor neuron L!, prevented habituation of the gill reflex or brought about its reversal in an already habituated preparation. Because the induced L,, activity did not affect the synaptic decrement in central gill motor neurons which normally accompanies reflex habituation (Kupfermann et al. 1970). it was proposed that Lo's effect occurred peripherally in the gill. Since LC,is dopaminergic (Swann et al. 1 9 7 8 ~ )and since dopamine has been shown to be an effective neuromuscular transmitter in the Aplysia gill (Ruben et al. 19771, it was thought that the perfusion of dopamine-containing seawater through the gill might also affect gilI reflex behaviors. It might also be a more direct test as to whether L,,'s effect occurs peripherally, as dopamine would only be permitted to act on the periphery. We now report that the perfusion of dopamine through the gill significantly potentiated the an~plitudeof the giIl withABBREVIATIONS:CNS, central nervous system; PNS, peripheral nervous system.
drawal reflex and prevented habituation of the reflex. These data indicatc that L9's effect on habituation occurs peripherally and that part of the CNS's facili t a t o r ~control is mediated via a dopaminergic path-
waF Methods Adysia californica weighing 150-250 g (obtained from Pacific Biornarine, Venice, CA), maintained in artificial seawater (Instant Ocean) at 15-16"C, pH 7.9, were used in these The preparation Was similar to that described previously and consisted of the siphon, mantle, gill, and abdominal ganglion (the CNS) (Lukowiak 1977, personal communication). The preparation was pinned out on a Sylgard base in a 200-mL Plexiglas bath filled with seawater (maintained at 16°C). The abdominal ganglion was isolated from the rest of the preparation in a leak-proof chamber with the ctenidinl, siphon, and branchial nerves intact. Thus, soiutio~lscould be perfused through the gill without coming into contact with the CNS. In order to perfuse the gill, the afferent vessel was cannulated and an incision made in the heart allowed the efflux of perftisate which w a s then ren~ovedfrom the bath by suction. Goncentrations of dopamine (Sigma) ranged from lW7 to 5 x 10 M. Dogamine was used within 5 min of preparation to avoid oxidation. The concentration used was based upon two criteria: ( I ) whether dopamine evoked movements similar to those produced by L, activity, and ( 2 ) whether dopamine potentiated the gill movement elicited by L7 activity (Swann et al. 1978a, 19780). The normal flow rate through the gill was 5 mL/min. Gill movements were measured by connecting a pinnule tip to a force transducer (Grass) with fine surgical thread (Peretz et al. 1976). Tactile stimuli (1000 mg) were delivered to the siphon by a mechanical tapper, a more complete description of which is given elsewhere (Peretz and Lukowiak 1975). Identified gill motor neurons were impaled with microelectrodes filled with 3 M KC1 ( 10-30 MO) and connected to a bridge circuit in an electrometer (Getting M5) which allowed simultaneous recording and stimulation.
0008-4212i79i030329-o4$01.~0 @ 1979 National Research Council of CanadaiConseil national de recherches du Canada
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
33 0
CAN. J. PI-IYSIOL. PHARMACOL. VOL. 57, 1939
FIG.2. Doparnine potentiation of gill withdrawal reflex. Bar graph represents the mean relative reflex amplitude to siphon stimulation during seawater (control) (SW) and dopamine-containing seawater (SW $ D A ) perfusion. The data from seven experiments were ncsrn~alizedwith control values at 100% The increase in the gill reflex amplitude is statistically significant during dopamine perfiasion. Standard errors are shown.
I. These data are consistent with previous results (Swann et al. 1978b). Using the same corncentration of dopamine, we determined what effect, if any, dopamine had on the gill withdrawal reflex evoked by tactile stirnulatiom of tbe siphon. As can be seen (Fig. 2), the amplitude of the gill withdrawal reflex was significantly increased ( t test; g < 0.01 ) by the perfusion of dopamine through the gill. The increase in the size of the contractions ranged ixa these experiments between 55 and 7 5 % . Despite the increase in reflex amplitude, the activity evoked in L 7 by the tactile stimulus of the siphon was not changed with dopalnine perfusion. Dopamine perfusion had no effect on the reflex latency. FIG.1. Dopamine potentiation of K-induced gill contracWe next studied the effects of dopamine perfusion tion. ( A ) Seawater was perfused through the gill at a flow on the habituation of the gill withdrawal reflex (Fig. rate of 5 rn%/min. Gill motor neuron L, was depolarized for 2.5 s to produce 15 action potentials, The gill contrac- 3 ) . With inorrnal seawater perfused through the gill, tion thus evoked is seen in the upper trace. ( B ) Seawater repeated tactile stimulation of the siphon (1000 mg; containing 2 x 10 A4 dopamine was perfused through the interstimulus interval 30 s) resulted in habituation gill. 1,, was depolarized to elicit the same number of spikes of the reflex. The synaptic input to L7, as evidenced as in ( A ) above. The subsequent gill contraction was greatly potentiated over the control response seen in ( A ) . by the number of action potentials evoked om each Time scale. 500 111s;upper trace, 200 nmg; lower trace, 20 mV. trial, also decremented as expected. Three hours later when dopamine-containing seawater was perResults fused through the gill, repetitive stimulation of the The perfusion of dopamine-containing seawater siphon did not result in habituation of the reflex. In through the gill evoked movements similar to those two experiments, a slight decrement was observed. produced by Ln stimulation. Moreover, the concen- but the rate of this decrement was significantly less trations of dopamine used potentiated the gill move- ( t test; p < 0.81) than in the control. Even though ment elicited by L7 activity. This can be seen in Fig. the reflex no longer habituated, the number of action
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
COMMUNICATION
5
10
TRIALS
FIG.3. Prevention of habituation by dopamine. The data from six experiments in which the gill withdrawal reflex was tested for habituation to repeated siphon stimulation are shown. In each experiment, the reflex was tested during and, 3 h later, during perfusion of seawater perfusion (). dopamine-containing seawater (0). Habituation was prevented during dopamine perfusion. Interstimulus interval (ISI) was 30 s. Standard errors are shown.
potentials in L, continued to decrement as in the control. Thus, perfusion of dopamine through the gill significantly potentiated the reflex amplitude, prevented reflex habituation, but did not affect the decrement of synaptic input to L 7 or other gill motor neurons.
33 B
(Lukowiak 1978a, 1978h), and since L n is dopaminergic (Swann et al. 1 9 7 8 ~ these ) ~ data support the proposal that L,'s effects are also occurring peripherally in the gill. Three different procedures have now been found which interfere with or prevent habituation of the gill withdrawal reflex while not affecting the synaptic decremental process to central gill motor neurons. Removal of the branchial nerve input to the gill (which carries CNS suppressive influence) resulted in facilitation of the reflex with repeated siphon stimuIation and not habituation (Lukowiak 1977). Secondly, induced low frequency tonic LC,activity had similar effects with repeated siphon stimulation (Lukowiak 1978a, 1978h). And thirdly, the perfusion of dopamine through the gill also prevented gill reflex habituation. In all three cases, the synaptic input to central gill motor neurons evoked by siphon stimulation continucd to decrement as in the control situations. All these data show that the synaptic decren~entalprocess which occurs between the central sensory neurons and gill motor neurons as a result of repetitive siphon stimulation (Castellucci et al. 1970) cannot be the only mechanism of gill reflex habituation in this preparation under the stimulus conditions employed. These data show that any analysis of the neural mechanisms of gill reflex habituation must consider the entire integrated CNS-PNS. The data further suggest that doparnineryic pathways from the abdominal ganglion to the gill may be the means by which the CNS exerts facilitatory control over the PNS. The results obtained with dopamine perfusion are similar to those obtained following the renloval of the CNS's suppressive influence (L~tkowiak1977). The sites and mechanisms by which dopamine exerts its influence aver gill behaviors are not known. Dopanline could be acting on: ( I ) the peripheral terminations of central efferents, (2) neurons in the peripheral nerve plexus, or ( 3 ) the gill n~uscleitself. The modulatoiy effects sf dopamine may be mediated through the action of cyclic nucleotides as has been suggested in this and other systems (Kebabian et al. 1977; Weiss et al. 1978). Future investigations will attempt to reveal the nature of dopalnine effects in the Aplysia gill.
Discussion The results presented here show that dopamine, a putative neurotransmitter, when perfused through the gill of Aply.~ia,significantly potentiated the gilI withdrawal reflex and prevented habituation of the Acknowledgments reflex. These effects occurred without any alteration of central gill motor neuron activity, indicating that The authors wish to thank J. Goldberg for useful dopamine effects occurred peripherally in the gill. discussions and editing of this manuscript. This reSince the results reported here are similar to those search was supported by the Medical Research obtained with induced low level tonic activity in L9 Council of Canada.
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
332
CAN. J. PKYSIOL. PHARMACOL. VOL. 57, 1979
CASTELLUCCI, a/., PINSKER, W.,KUPFERMANN, I., and KANDEL, E. R. 1970. Neuronal mechanisms of habituation and dishabituation of the gill withdrawal reflex in Aplysiu. Science, 167,1745-1748. KEBARIAN, 1'. R., KEBABIAN, Q. W., SWANN, J. W., and GARPENTER, D. 0. 1977. Cyclic AMP in Aplysici gill: Increases by putativc rmeurotransn-nitters. Neurosci. Abstr. 7, 557. KUPFERMANN, I., CASTELLUCCI, a/.> PINSKER, H., and KANDEL, E. R. 1970. Neuronal correlates of habituation and dishabituation of the gill withdrawal reflex in Aplysiu. Science, 167, 1743-1745. LUKOWIAK, K. 1977. CNS control of the PNS-mediated gill withdrawal reflex and its habituation. Can. J. Physiol. Pharmacol. 55, 1252-1262. --- 19780. Lg modulation of L7's elicited gill withdrawal response in Aplysiu. Brain Kes., in press. 19786. Induced Lg activity prevents habituation of the gill withdrawal refex evoked by siphon stimulation in Apl?,siu. Neurosci. Abstr. 8, 61 7. LUKOWIAK, K., and P ~ n ~ rR.z ,1977. The interaction between the central and peripheral nervous systenms in the mediation
of the gill withdrawal reflex behavior in Aplysitr. J. Camp. Physiol. 117, 219-244. PERETZ,B., JACKLET, J. W., and LUKOWIAK, K. 1976. Mabituation of reflexes in Ap/y,ria: Contribution crf the peripheral and central nervous systems. Science, 191, 396-399. PERETZ,B., and LUKOWIAK, K. 1975. Age-dependent CNS control of the habituating gill withdrawal reflex and of correlated activity in identified neurons in Aplvsia. J. Gomp. Physiol. 1Q3, 1-17. RUBEN,P., SWANN,J . W., and CARPENTER, D. 0. 1077. Actions of several putative neurotransmitters on the gill of Aplysia. Neurosci. Abstr. 7, 590. SWANN, J. W., SINRACK, C. N., and CARPENPER, D. 0. 1 9 7 8 ~ . Dopanline-induced muscle contractions and nmsdulatio~iof neuromuscular transn-aissiormin Aplysici. Brain Res., in press. 19786. Evidence for identitied dopanline motor neurons to the gill of Aplysi~z.Neurosci. Lett., in press. N'EISS, K. R., CBHEN,J. L., and KUPFEKMANN, 1. 1078. Modulatory control of buccal n-nusculatureby a serotonergic neuron (metacerebral cell) in .4plysica. J. Neurophysiol. 41(1), 181-203.
COMM UNIGATION
Dopamine modulation of gill reflex behavior in Aplysia PETER RUBENAND KENLUKOWIAK Division of PBlysiologicud Sciences, Utziversity of Calgury, Calgary, Alta., Canada T2N IN4
Received November 6 , 1978
RUBEN, P., and LUKOWIAK, K. 1979. Dopamine modulation of gill reflex behavior in Aplysia Can. J. Physiol. Pharmacol. 57, 329-332. We have studied the effects of dopamine on the gill withdrawal reflex evoked by tactile siphon stimulation in the margine mollusc Aplysia. Physiological concentratio~ssof dopamine (diluted in seawater) were perfused through the gill during siphon stimulation series. The amplitude of the reflex was potentiated by dopamine and habituation of the reflex was prevented. This occurred with no change in the activity evoked in central motor neurons. These results lead us to conclude that the dopaniinergic motor neuron L9is modulating habituation in the periphery and that the central nervous system facilitatory control of the peripheral nervous system may act via a dopaminergic pathway.
Introduction The gill withdrawal and its subsequent habituation evoked by repeated tactile stilnulation of the siohon has been shown to be mediated bv the integrated activity of the CNS and PNS ( ~ u k d w i a k and Peretz 1977). In the integrated system, the CNS exerts both facilitatorv and sumressive control over PNS-mediated adaptiGe gill rekkx behaviors (Per& et al. 1976; ~ ~ k 1977 ~ 1. ~ The i ~ balance k between the facilitatory and suppressive iilfiuences determines the reflex amplitude, latency, and rate of habituation. How and where the CNS exerts its control is not yet k~lown.Recently, Lukowiak ( 1978n, 1978b) has found that induced low level tonic activity in the gill motor neuron L!, prevented habituation of the gill reflex or brought about its reversal in an already habituated preparation. Because the induced L,, activity did not affect the synaptic decrement in central gill motor neurons which normally accompanies reflex habituation (Kupfermann et al. 1970). it was proposed that Lo's effect occurred peripherally in the gill. Since LC,is dopaminergic (Swann et al. 1 9 7 8 ~ )and since dopamine has been shown to be an effective neuromuscular transmitter in the Aplysia gill (Ruben et al. 19771, it was thought that the perfusion of dopamine-containing seawater through the gill might also affect gilI reflex behaviors. It might also be a more direct test as to whether L,,'s effect occurs peripherally, as dopamine would only be permitted to act on the periphery. We now report that the perfusion of dopamine through the gill significantly potentiated the an~plitudeof the giIl withABBREVIATIONS:CNS, central nervous system; PNS, peripheral nervous system.
drawal reflex and prevented habituation of the reflex. These data indicatc that L9's effect on habituation occurs peripherally and that part of the CNS's facili t a t o r ~control is mediated via a dopaminergic path-
waF Methods Adysia californica weighing 150-250 g (obtained from Pacific Biornarine, Venice, CA), maintained in artificial seawater (Instant Ocean) at 15-16"C, pH 7.9, were used in these The preparation Was similar to that described previously and consisted of the siphon, mantle, gill, and abdominal ganglion (the CNS) (Lukowiak 1977, personal communication). The preparation was pinned out on a Sylgard base in a 200-mL Plexiglas bath filled with seawater (maintained at 16°C). The abdominal ganglion was isolated from the rest of the preparation in a leak-proof chamber with the ctenidinl, siphon, and branchial nerves intact. Thus, soiutio~lscould be perfused through the gill without coming into contact with the CNS. In order to perfuse the gill, the afferent vessel was cannulated and an incision made in the heart allowed the efflux of perftisate which w a s then ren~ovedfrom the bath by suction. Goncentrations of dopamine (Sigma) ranged from lW7 to 5 x 10 M. Dogamine was used within 5 min of preparation to avoid oxidation. The concentration used was based upon two criteria: ( I ) whether dopamine evoked movements similar to those produced by L, activity, and ( 2 ) whether dopamine potentiated the gill movement elicited by L7 activity (Swann et al. 1978a, 19780). The normal flow rate through the gill was 5 mL/min. Gill movements were measured by connecting a pinnule tip to a force transducer (Grass) with fine surgical thread (Peretz et al. 1976). Tactile stimuli (1000 mg) were delivered to the siphon by a mechanical tapper, a more complete description of which is given elsewhere (Peretz and Lukowiak 1975). Identified gill motor neurons were impaled with microelectrodes filled with 3 M KC1 ( 10-30 MO) and connected to a bridge circuit in an electrometer (Getting M5) which allowed simultaneous recording and stimulation.
0008-4212i79i030329-o4$01.~0 @ 1979 National Research Council of CanadaiConseil national de recherches du Canada
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
33 0
CAN. J. PI-IYSIOL. PHARMACOL. VOL. 57, 1939
FIG.2. Doparnine potentiation of gill withdrawal reflex. Bar graph represents the mean relative reflex amplitude to siphon stimulation during seawater (control) (SW) and dopamine-containing seawater (SW $ D A ) perfusion. The data from seven experiments were ncsrn~alizedwith control values at 100% The increase in the gill reflex amplitude is statistically significant during dopamine perfiasion. Standard errors are shown.
I. These data are consistent with previous results (Swann et al. 1978b). Using the same corncentration of dopamine, we determined what effect, if any, dopamine had on the gill withdrawal reflex evoked by tactile stirnulatiom of tbe siphon. As can be seen (Fig. 2), the amplitude of the gill withdrawal reflex was significantly increased ( t test; g < 0.01 ) by the perfusion of dopamine through the gill. The increase in the size of the contractions ranged ixa these experiments between 55 and 7 5 % . Despite the increase in reflex amplitude, the activity evoked in L 7 by the tactile stimulus of the siphon was not changed with dopalnine perfusion. Dopamine perfusion had no effect on the reflex latency. FIG.1. Dopamine potentiation of K-induced gill contracWe next studied the effects of dopamine perfusion tion. ( A ) Seawater was perfused through the gill at a flow on the habituation of the gill withdrawal reflex (Fig. rate of 5 rn%/min. Gill motor neuron L, was depolarized for 2.5 s to produce 15 action potentials, The gill contrac- 3 ) . With inorrnal seawater perfused through the gill, tion thus evoked is seen in the upper trace. ( B ) Seawater repeated tactile stimulation of the siphon (1000 mg; containing 2 x 10 A4 dopamine was perfused through the interstimulus interval 30 s) resulted in habituation gill. 1,, was depolarized to elicit the same number of spikes of the reflex. The synaptic input to L7, as evidenced as in ( A ) above. The subsequent gill contraction was greatly potentiated over the control response seen in ( A ) . by the number of action potentials evoked om each Time scale. 500 111s;upper trace, 200 nmg; lower trace, 20 mV. trial, also decremented as expected. Three hours later when dopamine-containing seawater was perResults fused through the gill, repetitive stimulation of the The perfusion of dopamine-containing seawater siphon did not result in habituation of the reflex. In through the gill evoked movements similar to those two experiments, a slight decrement was observed. produced by Ln stimulation. Moreover, the concen- but the rate of this decrement was significantly less trations of dopamine used potentiated the gill move- ( t test; p < 0.81) than in the control. Even though ment elicited by L7 activity. This can be seen in Fig. the reflex no longer habituated, the number of action
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
COMMUNICATION
5
10
TRIALS
FIG.3. Prevention of habituation by dopamine. The data from six experiments in which the gill withdrawal reflex was tested for habituation to repeated siphon stimulation are shown. In each experiment, the reflex was tested during and, 3 h later, during perfusion of seawater perfusion (). dopamine-containing seawater (0). Habituation was prevented during dopamine perfusion. Interstimulus interval (ISI) was 30 s. Standard errors are shown.
potentials in L, continued to decrement as in the control. Thus, perfusion of dopamine through the gill significantly potentiated the reflex amplitude, prevented reflex habituation, but did not affect the decrement of synaptic input to L 7 or other gill motor neurons.
33 B
(Lukowiak 1978a, 1978h), and since L n is dopaminergic (Swann et al. 1 9 7 8 ~ these ) ~ data support the proposal that L,'s effects are also occurring peripherally in the gill. Three different procedures have now been found which interfere with or prevent habituation of the gill withdrawal reflex while not affecting the synaptic decremental process to central gill motor neurons. Removal of the branchial nerve input to the gill (which carries CNS suppressive influence) resulted in facilitation of the reflex with repeated siphon stimuIation and not habituation (Lukowiak 1977). Secondly, induced low frequency tonic LC,activity had similar effects with repeated siphon stimulation (Lukowiak 1978a, 1978h). And thirdly, the perfusion of dopamine through the gill also prevented gill reflex habituation. In all three cases, the synaptic input to central gill motor neurons evoked by siphon stimulation continucd to decrement as in the control situations. All these data show that the synaptic decren~entalprocess which occurs between the central sensory neurons and gill motor neurons as a result of repetitive siphon stimulation (Castellucci et al. 1970) cannot be the only mechanism of gill reflex habituation in this preparation under the stimulus conditions employed. These data show that any analysis of the neural mechanisms of gill reflex habituation must consider the entire integrated CNS-PNS. The data further suggest that doparnineryic pathways from the abdominal ganglion to the gill may be the means by which the CNS exerts facilitatory control over the PNS. The results obtained with dopamine perfusion are similar to those obtained following the renloval of the CNS's suppressive influence (L~tkowiak1977). The sites and mechanisms by which dopamine exerts its influence aver gill behaviors are not known. Dopanline could be acting on: ( I ) the peripheral terminations of central efferents, (2) neurons in the peripheral nerve plexus, or ( 3 ) the gill n~uscleitself. The modulatoiy effects sf dopamine may be mediated through the action of cyclic nucleotides as has been suggested in this and other systems (Kebabian et al. 1977; Weiss et al. 1978). Future investigations will attempt to reveal the nature of dopalnine effects in the Aplysia gill.
Discussion The results presented here show that dopamine, a putative neurotransmitter, when perfused through the gill of Aply.~ia,significantly potentiated the gilI withdrawal reflex and prevented habituation of the Acknowledgments reflex. These effects occurred without any alteration of central gill motor neuron activity, indicating that The authors wish to thank J. Goldberg for useful dopamine effects occurred peripherally in the gill. discussions and editing of this manuscript. This reSince the results reported here are similar to those search was supported by the Medical Research obtained with induced low level tonic activity in L9 Council of Canada.
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by GRANT MACEWAN UNIV on 11/14/14 For personal use only.
332
CAN. J. PKYSIOL. PHARMACOL. VOL. 57, 1979
CASTELLUCCI, a/., PINSKER, W.,KUPFERMANN, I., and KANDEL, E. R. 1970. Neuronal mechanisms of habituation and dishabituation of the gill withdrawal reflex in Aplysiu. Science, 167,1745-1748. KEBARIAN, 1'. R., KEBABIAN, Q. W., SWANN, J. W., and GARPENTER, D. 0. 1977. Cyclic AMP in Aplysici gill: Increases by putativc rmeurotransn-nitters. Neurosci. Abstr. 7, 557. KUPFERMANN, I., CASTELLUCCI, a/.> PINSKER, H., and KANDEL, E. R. 1970. Neuronal correlates of habituation and dishabituation of the gill withdrawal reflex in Aplysiu. Science, 167, 1743-1745. LUKOWIAK, K. 1977. CNS control of the PNS-mediated gill withdrawal reflex and its habituation. Can. J. Physiol. Pharmacol. 55, 1252-1262. --- 19780. Lg modulation of L7's elicited gill withdrawal response in Aplysiu. Brain Kes., in press. 19786. Induced Lg activity prevents habituation of the gill withdrawal refex evoked by siphon stimulation in Apl?,siu. Neurosci. Abstr. 8, 61 7. LUKOWIAK, K., and P ~ n ~ rR.z ,1977. The interaction between the central and peripheral nervous systenms in the mediation
of the gill withdrawal reflex behavior in Aplysitr. J. Camp. Physiol. 117, 219-244. PERETZ,B., JACKLET, J. W., and LUKOWIAK, K. 1976. Mabituation of reflexes in Ap/y,ria: Contribution crf the peripheral and central nervous systems. Science, 191, 396-399. PERETZ,B., and LUKOWIAK, K. 1975. Age-dependent CNS control of the habituating gill withdrawal reflex and of correlated activity in identified neurons in Aplvsia. J. Gomp. Physiol. 1Q3, 1-17. RUBEN,P., SWANN,J . W., and CARPENTER, D. 0. 1077. Actions of several putative neurotransmitters on the gill of Aplysia. Neurosci. Abstr. 7, 590. SWANN, J. W., SINRACK, C. N., and CARPENPER, D. 0. 1 9 7 8 ~ . Dopanline-induced muscle contractions and nmsdulatio~iof neuromuscular transn-aissiormin Aplysici. Brain Res., in press. 19786. Evidence for identitied dopanline motor neurons to the gill of Aplysi~z.Neurosci. Lett., in press. N'EISS, K. R., CBHEN,J. L., and KUPFEKMANN, 1. 1078. Modulatory control of buccal n-nusculatureby a serotonergic neuron (metacerebral cell) in .4plysica. J. Neurophysiol. 41(1), 181-203.
