| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
REPORT
1Laboratory of Neurobiophysics, School of Pharmaceutical Sciences, The University of Tokyo, Tokyo; and 2 Department of Information Physiology, National Institute for Physiological Sciences, Okazaki, Japan
Submitted 15 August 2005; accepted in final form 20 February 2006
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
; Freeman 1978; Gelperin and Tank 1990; Laurent and Davidowitz 1994; Laurent and Naraghi 1994). Such network oscillations are generated by synchronous oscillation of electrical activities among numerous neurons in olfactory systems. The role of these network oscillations in olfactory information processing has been explored in invertebrate olfactory systems, especially in insect olfactory systems (for review see Laurent 2002).
One important advantage of molluscan nervous systems is that molluscan brains in vitro retain several types of computational properties found in vivo (e.g., learning and memory and central pattern generator). These in vitro preparations enable us to conduct complicated electrophysiological recordings. The procerebrum (PC) is the olfactory center of Limax and related species (Chase 1985). The PC consists of 105 neurons and exhibits ongoing network oscillation even in vitro (Gelperin and Tank 1990; Kleinfeld et al. 1994). The network oscillations are analogous to the network oscillation in vivo (Cooke and Gelperin 2001). The network oscillations in the PC are modulated in response to odor application to the nose (Delaney et al. 1994; Gelperin and Tank 1990; Kimura et al. 1998b). In addition, odor application to the noses produces discharges in efferent nerves of in vitro preparations (Gervais et al. 1996; Inoue et al. 2004; Teyke and Gelperin 1999).
Limax has abilities of odor learning in vivo (Kimura et al. 1998a; Sahley et al. 1981). However, it is still unclear whether abilities of odor learning are preserved in vitro. Can isolated brains, containing the nose and motor output, acquire memories of odors? Several types of in vitro conditioning systems have been reported using other molluscan nervous systems: classical conditioning of the gill-withdrawal reflex system in Aplysia (Lukowiak and Sahley 1981); classical conditioning in feeding systems in Limax (Chang and Gelperin 1980), Lymnaea (Kemenes et al. 1997), and Aplysia (Mozzachiodi et al. 2003; Reyes et al. 2005); and operant conditioning in feeding systems in Aplysia (Nargeot et al. 1997). However, there have been no reports of in vitro conditioning in olfactory systems. Such a system would enable us to study the role of network oscillation in olfactory information processing and olfactory learning. In this study, we report an ability of odor learning in in vitro preparations of Limax. Using this in vitro odor-aversion conditioning system, we also show that network oscillation frequency in the PC increases specifically in response to aversively conditioned and innately aversive odors, both of which elicit avoidance behavior.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
We used laboratory-bred slugs, Limax marginatus, whose body weight was 0.5–1.0 g. The brain, containing the nose (for application of conditioned stimulus [CS]), the lip and pedal nerves (for unconditioned stimulus [UCS] application), and the parietal nerve (for motor output observation), was isolated from each slug. The isolated brains were placed in physiological saline containing (in mM): 70 NaCl, 2 KCl, 4.7 MgCl2, 4.9 CaCl2, 5.0 glucose, 5.0 HEPES/Na, adjusted to pH 7.6 (Inoue et al. 2004). Extracellular recordings of the parietal nerve were made with a conventional glass suction electrode (150–1,000 Hz, band-pass filtered), and local field potential (LFP) recordings in the PC were made with a fine glass electrode (0.08–30 Hz, band-pass filtered). We waited for about 2 h for recovery from dissection. All experiments were performed at room temperature (20–25°C).
In vitro odor-aversion conditioning
We used two natural odorants, carrot and cucumber, as CS odors. The two odorants are both natively attractive to Limax (Kimura et al. 1998a). The odors were delivered to the nose pad in air, using an odor stimulator (Inoue et al. 2004). For the UCS, two afferent nerves, the external lip nerve (ELn) and the anterior pedal nerve (APn), were electrically stimulated (5 V, 6.67 Hz, 15 s) using glass suction electrodes. Electrical stimulation of these nerves is an adequate UCS for in vitro conditioning of Limax because Limax can be aversively conditioned by electrical stimulation of the anterior–dorsal parts of the body in vivo (Fig. 1). During aversive conditioning, one odor was paired with the UCS and the other odor was unpaired with the UCS in the same preparations (differential conditioning; see Fig. 2B). The paired odor was referred to as the CS+ and the unpaired odor was referred to as the CS– in the text and figure legends. The conditioned response (CR) was quantified as the number of posterior viceral neuron (p-VN) spikes, which were extracellularly recorded from the left parietal nerves. To identify p-VN spikes in the left parietal nerves, we touched the nose pad before the pretest period (see Fig. 2B), and observed fully evoked discharges in the left parietal nerves. These evoked discharges had larger amplitudes than those of spontaneous discharges, and the larger discharges were classified into several units (basically two units) based on the distinguishable amplitudes. A unit of maximum-amplitude spikes in the left parietal nerve was regarded as p-VN spikes in this study, as previously reported (Inoue et al. 2004).
|
|
The normalized mantle length in Fig. 1C was calculated as previously described (Inoue et al. 2004). Briefly, after the conditioning, the mantle lengths (see Fig. 1B) at three arbitrary time points during spontaneous behavior were measured and averaged (defined as the averaged length). The mantle lengths just before and during odor presentation were then measured and normalized to the averaged length (defined as the normalized mantle length in Fig. 1C). In Fig. 2, spiking activity in the p-VN was defined as the number of p-VN spikes during 15-s odor-stimulus periods followed by subtraction of the number of p-VN spikes during 15-s preodor periods. The index of learning (IOL) in Fig. 3 was defined as (CSpost+ – CSpost–) – (CSpre+ – CSpre–), in which CSpost+ or CSpre+ (CSpost– or CSpre–) indicates the spiking activity of the p-VN in response to CS+ odor (CS– odor) after or before the in vitro conditioning, respectively. Thus a positive change in the IOL indicates that the isolated brains show odor-aversion learning more clearly. All quantitative data were represented as means ± SE. For statistical analyses of the difference between before and after odor application, two-tailed paired t-tests were used (*P < 0.05, **P < 0.01, n.s., not significant).
|
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
Limax is known to have an ability of odor learning (Kimura et al. 1998a; Sahley et al. 1981). After odor-aversion conditioning, Limax exhibits avoidance behavior in response to natively attractive but aversively conditioned odors. However, the neural components governing this odor-induced avoidance behavior remain unclear. Identification of the neural components is essential to reproducing odor-aversion conditioning in vitro. To identify the neural components, we first examined the muscle movement of Limax during odor-induced avoidance behavior in vivo.
We applied a differential conditioning paradigm, where two different odors (carrot and cucumber) were used. Because both odors are natively attractive odors for Limax (Kimura et al. 1998a), the animals approached these odorants (Before conditioning in Fig. 1A). During the differential conditioning, one odor (CS+) was paired with a noxious electrical stimulus (UCS; During conditioning in Fig. 1A), and then the other odor (CS–) alone was applied to the same animals 1 h after CS+–UCS pairing. One hour is too long to pair the CS– and UCS. After the conditioning, they exhibited withdrawal behavior from the CS+ odorant, but still exhibited an approach behavior to the CS– odorant (After conditioning in Fig. 1A). During the withdrawal behavior from the CS+ odorant, shortening of the mantle muscle was observed (Mantle in Fig. 1B).
We quantitatively measured changes in the length of the mantle muscle in response to odors after the differential conditioning (Fig. 1C). After one time pairing, we applied the CS+ odor and CS– odor to each animal. In the cucumber-conditioned group (Fig. 1C; n = 5 slugs), the mantle shortening was observed in response to the CS+ cucumber odor (74.7 ± 3.4% of the control, n = 5; P < 0.01), but not in response to the CS– carrot odor (92.6 ± 7.5% of the control, n = 5; P > 0.05). By contrast, in the carrot-conditioned group (Fig. 1C; n = 5 slugs), the mantle shortening was observed in response to the CS+ carrot odor (74.6 ± 8.4% of the control, n = 5; P < 0.05), but not in response to the CS– cucumber odor (89.6 ± 12.1% of the control, n = 5; P > 0.05). These results indicate that shortening of the mantle muscle is associated with the avoidance behavior in response to aversively conditioned odors.
The parietal nerves connect the mantle muscle to the brain and carry motor and sensory information (Pn in Fig. 1B). We previously reported that lesioning of the parietal nerves in vivo completely blocked repellent odor-induced shortening of the mantle muscle (Inoue et al. 2004), which indicates that the parietal nerves regulate odor-induced shortening of the mantle muscle. Discharges in the parietal nerves are spontaneously generated in vitro, but larger-amplitude discharges in the parietal nerves are observed in response to natively aversive odors (Inoue et al. 2004). Such larger-amplitude discharges are not observed in response to attractive odors (Inoue et al. 2004). We therefore used the discharges in the parietal nerves, as an in vitro index of odor-induced avoidance behavior, in the following in vitro experiments (Figs. 2–4).
|
We next examined whether the nose–brain–parietal nerve preparations were aversively conditioned, using the in vitro index of avoidance behavior (Fig. 2). The nose–brain–parietal nerve preparations and stimulating/recording electrodes are shown in Fig. 2A. The conditioning paradigm in vitro (Fig. 2B) is a differential conditioning paradigm similar to that used in vivo, except that the experiments in Fig. 2 were performed using isolated brains. One advantage of this conditioning paradigm is that both paired and unpaired odors can be tested in the same in vitro preparation.
In the isolated preparations, attractive odors (cucumber and carrot) elicited no change in discharges of the parietal nerve (first and second traces in Fig. 2C). However, after one time pairing between the attractive cucumber odor (paired odor; CS+) and electrical stimulation of ELn and APn (UCS), application of the same cucumber odor elicited larger-amplitude discharges in the parietal nerve (third and fifth traces in Fig. 2C). Unpaired carrot odor (CS–) did not elicit the discharges (fourth and sixth traces in Fig. 2C). Thus the isolated brain selectively produces the large-amplitude discharges in the parietal nerve (i.e., an in vitro index of avoidance behavior) in response to the aversively conditioned cucumber odor.
To quantify the effect of the in vitro odor-aversion conditioning, we counted the spikes in the p-VN, which is a motoneuron projecting its axon into the parietal nerves and innervating the mantle muscle (Inoue et al. 2004). The p-VN spikes could be readily identified by extracellular recording of the left parietal nerves (indicated by horizontal arrowheads in Fig. 2C; see METHODS). In the cucumber-conditioned brains (Fig. 2D), the spiking activity in the p-VN increased in response to the cucumber odor (spiking activity before conditioning 
spiking activity after conditioning; 0.41 ± 0.22 3.35 ± 1.02, n = 17; P < 0.01), whereas the spiking activity did not change in response to the carrot odor (0.41 ± 0.25 0.53 ± 0.28, n = 17; P > 0.05).
To establish whether the changes in spiking activity were indeed conditioning dependent, a control experiment was performed. In this experiment, we used carrot odor as the CS+ (paired) odor, and cucumber odor as the CS– (unpaired) odor. In the carrot-conditioned group (Fig. 2D), the spiking activity increased in response to the paired carrot odor (0.35 ± 0.15 2.53 ± 0.66, n = 17; P < 0.01), whereas the spiking activity did not change in response to the unpaired cucumber odor (0.18 ± 0.10 0.53 ± 0.28, n = 17; P > 0.05). These results indicate that the nose–brain–parietal nerve preparations could be aversively conditioned, using an in vitro index of avoidance behavior.
Changes in the PC network oscillation after in vitro odor-aversion conditioning
The PC consists of 105 neurons, and this large population of neurons spontaneously exhibits regular synchronized oscillation at about 0.7 Hz (Gelperin and Tank 1990). The synchronized oscillation can be recorded as oscillations of the local field potential (LFP) in the PC (Gelperin and Tank 1990). We performed simultaneous recordings of discharges in the p-VN and LFP oscillations in the PC (Fig. 3).
As shown in Fig. 2C, application of attractive cucumber and carrot odors to the nose hardly changed the pattern of discharges in the p-VN. LFP oscillations in the PC also hardly changed in response to these attractive odors (Before conditioning in Fig. 3, A and B). However, after the cucumber odor was paired with the UCS, application of the cucumber odor increased the PC oscillation frequency approximately twofold (After conditioning in Fig. 3, A and B), and elicited p-VN spikes (indicated by horizontal arrowheads in Fig. 3A). The unpaired carrot odor did not change the PC oscillation frequency even after conditioning. We then quantitatively analyzed the odor-evoked change in the LFP frequency, in a series of the in vitro odor-aversion conditioning experiments (Fig. 3C). After the in vitro conditioning, the aversively conditioned odors selectively increased the frequency of LFP oscillation (CS+ after conditioning, 127.1 ± 8.2% of the baseline frequency, n = 20; P < 0.01). The frequency of LFP oscillation was not modulated by the unpaired odors (CS– after conditioning, 104.4 ± 2.9% of the baseline frequency, n = 20; P > 0.05).
We then studied the relationship between the conditioned odor-evoked increase in the PC oscillation frequency and the index of learning (IOL; see METHODS). Figure 3D shows plots of the change in the conditioned odor-evoked LFP frequency, against the IOL (n = 20). We observed a moderate positive correlation, where the correlation coefficient was 0.57 (Fig. 3D). In Fig. 3E, we classified the conditioned isolated brains (n = 20) into good-learner (n = 7/20) and poor-learner (n = 13/20) preparations, based on the IOL. The IOL classification revealed that the increase in PC oscillation frequency after conditioning was observed only in the good-learner group (Fig. 3E; 153.9 ± 15.9% after conditioning; n = 7, P < 0.05), but not in the poor-learner group (Fig. 3E; 112.7 ± 7.1% after conditioning; n = 13, P > 0.05). These results clearly show that the frequency of the PC network oscillation is correlated with discharges in the p-VN, an in vitro index of odor-avoidance behavior.
Changes in the PC oscillation frequency in response to natively aversive odors
There are two possible explanations for the selective increase in PC oscillation frequency in response to aversively conditioned odors. One is that the increase is correlated with the aversion to the applied odor and the other is that the increase is correlated with the learning of the applied odor. To address this issue, we applied two types of natively aversive odors (onion and garlic) and two types of natively attractive odors (potato and rat chow) to naive preparations that had not received any conditioning (Fig. 4).
We previously showed that mantle shortening of Limax in vivo was selectively induced by the two natively aversive odors, onion and garlic (Inoue et al. 2004). Our in vitro study has also revealed that spikes in the p-VN were generated by the two aversive odors, but were not induced by the two natively attractive odors (Inoue et al. 2004; also see Pn in Fig. 4A). As shown in Fig. 4A in which onion and potato odors were applied to a naive preparation, the PC oscillation frequency increased specifically in response to the aversive onion odor. Quantitative analysis (Fig. 4B; n = 5) revealed that the PC oscillation frequency increased in response to the aversive onion odor (149.5 ± 14.8% of the baseline frequency, n = 5; P < 0.05), but hardly increased in response to the attractive potato odor (111.1 ± 7.4% of the baseline frequency, n = 5; P > 0.05). In another set of preparations to which garlic and rat chow odors were applied (Fig. 4B; n = 5), the PC oscillation frequency increased in response to the aversive garlic odor (137.1 ± 11.1% of the baseline frequency, n = 5; P < 0.05), but hardly increased in response to the attractive rat chow odor (108.8 ± 6.5% of the baseline frequency, n = 5; P > 0.05). These results indicate that odor-induced increases in PC oscillation frequency are correlated with the aversion to the applied odor.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
Molluscan nervous systems are useful preparations for studying the dynamics and function of neuronal circuits because molluscan brains containing sensory and motor organs can carry out several types of computations, such as learning and memory, even in artificial Ringer solution. To study the mechanism of learning and memory at the circuit level, several types of in vitro conditioning systems have been developed, such as classical conditioning of the gill withdrawal reflex in Aplysia (Lukowiak and Sahley 1981); classical conditioning in the feeding system of Limax (Chang and Gelperin 1980), Lymnaea (Kemenes et al. 1997), and Aplysia (Mozzachiodi et al. 2003; Reyes et al. 2005); and operant conditioning in the feeding system of Aplysia (Nargeot et al. 1997). The study on the gill-withdrawal system has focused on conditioning-dependent synaptic changes, and studies on the feeding system have also focused on conditioning-dependent changes in central pattern generator circuits. In this study, we reported conditioning-dependent changes in network oscillations in olfactory systems, using the in vitro odor-aversion conditioning system.
The PC exhibits ongoing network oscillations in vitro (Gelperin and Tank 1990; Kleinfeld et al. 1994) and in vivo (Cooke and Gelperin 2001). In in vitro preparations, it has been shown that application of odors to the nose modulates the frequency of PC network oscillations (Gelperin and Tank 1990; Gervais et al. 1996; Kimura et al. 1998b). These studies have shown that attractive odors and aversive odors exhibit distinct patterns of change in the PC oscillation frequency. However, it has been unknown whether different patterns of frequency change are coupled with different patterns of behavioral output. In this study, we found that oscillation frequency in the PC increased specifically in response to aversively conditioned odors (Fig. 3C). We then found that the increase in PC oscillation frequency was correlated with discharges in the p-VN, an in vitro index of odor-avoidance behavior (Fig. 3, D and E). We also found that, in naive preparations, increases in PC oscillation frequency were observed in response to natively aversive odors but not to natively attractive ones (Fig. 4). Thus changes in PC oscillation frequency are associated specifically with odors that elicit avoidance behavior, both aversively conditioned odors and natively aversive odors.
Although our experiments showed that increases in PC oscillation frequency were strongly correlated with the aversion to the applied odors, we could not directly demonstrate a causal relationship by lesioning of the PC. This is partially the result of a technical difficulty: we should maintain the viability of the in vitro preparations throughout the series of in vitro conditioning experiments (
5 h after dissection). However, odor-induced neural responses were progressively reduced by lesioning of the PC or removal of sheaths surrounding the PC. Thus it will be necessary to develop more viable in vitro preparations, to directly examine the causal relationship.
Studies on the insect olfactory system have revealed that discrimination of closely related odors is impaired by blockage of synchronized activity in the antennal lobe (MacLeod et al. 1998; Stopfer et al. 1997). Network oscillation in the PC is also involved in discriminating closely related odors in Limax (Teyke and Gelperin 1999). In this study, we propose that network oscillation in the PC is involved in the aversion of odors. Thus it is assumed that the PC network oscillation is involved in different types of olfactory processing: discrimination between closely related odors and discrimination between aversive and attractive odors. It will be interesting to explore the neural mechanism underlying the different types of olfactory processing.
Then, how does the increase in PC oscillation frequency generate discharges in the p-VN? We previously found an identifiable serotonergic neuron, the posterior cerebral serotonergic cell (p-CSC; Inoue et al. 2004). Discharges in the p-CSC released serotonin in the tentacle ganglion (TG). Serotonin in the TG suppressed aversive odor-induced discharges in the p-VN (Inoue et al. 2004). These previous findings suggest that the p-CSC may be a neuron that regulates odor-induced p-VN discharges. Our preliminary studies revealed that pharmacological manipulation of the PC modulated the firing rate of the p-CSC; increase of PC oscillation frequency by acetylcholine (Watanabe et al. 2001) decreased the p-CSC firing rate (Inoue et al., unpublished observations). These preliminary studies suggest that there may be a pathway from the PC to the p-CSC. We have not yet succeeded in making intracellular recordings of the p-CSC throughout the in vitro conditioning paradigm. The approach will enable us to directly examine the neural mechanism that the oscillation frequency in the PC mediates odor-guided avoidance behavior.
|
GRANTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
|
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: Y. Kirino, Laboratory of Neurobiophysics, School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan (E-mail: kirino{at}mayqueen.f.u-tokyo.ac.jp)
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
Chang JJ and Gelperin A. Rapid taste-aversive learning by an isolated molluscan central nervous system. Proc Natl Acad Sci USA 77: 6204–6206, 1980.
Chase R. Responses to odors mapped in snail tentacle and brain by [14C]-2-deoxyglucose autoradiography. J Neurosci 5: 2930–2939, 1985.[Abstract]
Cooke IR and Gelperin A. In vivo recordings of spontaneous and odor-modulated dynamics in the Limax olfactory lobe. J Neurobiol 46: 126–141, 2001.[CrossRef][ISI][Medline]
Delaney KR, Gelperin A, Fee MS, Flores JA, Gervais R, Tank DW, and Kleinfeld D. Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc Natl Acad Sci USA 91: 669–673, 1994.
Freeman WJ. Spatial properties of an EEG event in the olfactory bulb and cortex. Electroencephalogr Clin Neurophysiol 44: 586–605, 1978.[CrossRef][ISI][Medline]
Gelperin A and Tank DW. Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345: 437–440, 1990.[CrossRef][Medline]
Gervais R, Kleinfeld D, Delaney KR, and Gelperin A. Central and reflex neuronal responses elicited by odor in a terrestrial mollusk. J Neurophysiol 76: 1327–1339, 1996.
Inoue T, Inokuma Y, Watanabe S, and Kirino Y. In vitro study of odor-evoked behavior in a terrestrial mollusk. J Neurophysiol 91: 372–-381, 2004.
Kemenes G, Staras K, and Benjamin PR. In vitro appetitive classical conditioning of the feeding response in the pond snail Lymnaea stagnalis. J Neurophysiol 78: 2351–2362, 1997.
Kimura T, Suzuki H, Kono E, and Sekiguchi T. Mapping of interneurons that contribute to food aversive conditioning in the slug brain. Learn Mem 4: 376–388, 1998a.
Kimura T, Toda S, Sekiguchi T, and Kirino Y. Behavioral modulation induced by food odor aversive conditioning and its influence on the olfactory responses of an oscillatory brain network in the slug Limax marginatus. Learn Mem 4: 365–375, 1998b.
Kleinfeld D, Delaney KR, Fee MS, Flores JA, Tank DW, and Gelperin A. Dynamics of propagating waves in the olfactory network of a terrestrial mollusk: an electrical and optical study. J Neurophysiol 72: 1402–1419, 1994.
Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3: 884–895, 2002.[CrossRef][ISI][Medline]
Laurent G and Davidowitz H. Encoding of olfactory information with oscillating neural assemblies. Science 265: 1872–1875, 1994.
Laurent G and Naraghi M. Odorant-induced oscillations in the mushroom bodies of the locust. Neuroscience 14: 2993–3004, 1994.[Abstract]
Lukowiak K and Sahley C. The in vitro classical conditioning of a gill withdrawal reflex in Aplysia: neural correlates and possible neural mechanisms. Science 212: 1516–1518, 1981.
MacLeod K, Backer A, and Laurent G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395: 693–698, 1998.[CrossRef][Medline]
Mozzachiodi R, Lechner HA, Baxter DA, and Byrne JH. In vitro analog of classical conditioning of feeding behavior in Aplysia. Learn Mem 10: 478–494, 2003.
Nargeot R, Baxter DA, and Byrne JH. Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J Neurosci 17: 8093–8105, 1997.
Reyes FD, Mozzachiodi R, Baxter DA, and Byrne JH. Reinforcement in an in vitro analog of appetitive classical conditioning of feeding behavior in Aplysia: blockade by a dopamine antagonist. Learn Mem 12: 216–220, 2005.
Sahley C, Gelperin A, and Rudy JW. One-trial associative learning modifies food odor preferences of a terrestrial mollusk. Proc Natl Acad Sci USA 78: 640–642, 1981.
Stopfer M, Bhagavan S, Smith BH, and Laurent G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390: 70–74, 1997.[CrossRef][Medline]
Teyke T and Gelperin A. Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. Neuroreport 10: 1061–1068, 1999.[ISI][Medline]
Watanabe S, Inoue T, Murakami M, Inokuma Y, Kawahara S, and Kirino Y. Modulation of oscillatory neural activities by cholinergic activation of interneurons in the olfactory center of a terrestrial slug. Brain Res 896: 30–35, 2001.[CrossRef][ISI][Medline]
This article has been cited by other articles:
|
|
 |
|
  S. Watanabe, Y. Kirino, and A. Gelperin Neural and molecular mechanisms of microcognition in Limax Learn. Mem., August 26, 2008; 15(9): 633 - 642. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Kasai, S. Watanabe, Y. Kirino, and R. Matsuo The procerebrum is necessary for odor-aversion learning in the terrestrial slug Limax valentianus Learn. Mem., July 1, 2006; 13(4): 482 - 488. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
