Complex responses to light of the nudibranch Hermissenda crassicornis (Gastropoda: opisthobranchia)

Lederhendler, Izja; Barnes, Edward S.; Alkon, Daniel L.

doi:10.1016/s0163-1047(80)91599-x

Cited by 19 publications

(12 citation statements)

References 29 publications

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“…Our development and refinement of the open-field test (Lederhendler et al, 1980) was prompted by our inability to demonstrate enhanced phototaxis (decreased response latencies) for the EUtrained animals using the conventional straight-tube tests of phototaxis that have been used in the majority of studies with Hermissenda Alkon, 1978, 1980;Alkon, 1982, 1987). During pretraining straight-tube tests of phototaxis, animals are already moving quite rapidly, making it difficult to observe f urther decreases in baseline latencies.…”

Section: Discussionmentioning

confidence: 99%

Behavioral and Neural Bases of Noncoincidence Learning inHermissenda

Britton

Farley

1999

J. Neurosci.

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Neurobiological studies of associative learning and memory have focused nearly exclusively on the analysis of neural plasticity resulting from paired stimuli. A second major category of associative-learning processes, one that has been conspicuously neglected in cellular studies, is that of conditioned inhibition (CI), learning that one stimulus signals the absence of another. The physiological bases of CI are obscure and unexplored. To study the behavioral and neural bases of CI, we exposed the nudibranch mollusc Hermissenda crassicornis to explicitly unpaired (EU) presentations of light and rotation. We report here that Hermissenda exhibited persistent increases in phototactic behavior after EU training. Retardation-of-learning test results provided further evidence that EU animals learned that light signaled the absence of rotation. The increased phototactic behavior of EU animals was paralleled by selective decreases in the magnitude of ocular type B cell photoresponses and the frequency of light-elicited action potentials: the first report of a neural correlate of noncoincidence learning. Plasticity arising from explicitly unpaired stimulus presentations raises provocative questions as to how noncoincidence is detected and represented within the nervous system. Key words: learning and memory; Hermissenda; conditioned inhibition; photoreceptors; rotation; noncoincidenceNeurobiological studies of associative learning and memory (Woody, 1986;Byrne, 1987;Krasne and Glanzmann, 1996) and presumptive neurophysiological models of these processes (Bliss and Collingridge, 1993;Linden and Connor, 1995) have focused nearly exclusively on the analysis of neural plasticity resulting from the presentation of temporally contiguous stimuli (pairedstimulation paradigms). In classical conditioning experiments, such procedures are exemplified by conditioning trials in which conditioned (C S) and unconditioned (US) stimuli are paired with one another, as in so-called conditioned excitation training paradigms.A second major category of associative-learning processes, one that has been conspicuously neglected in cellular studies of learning and memory, is that of conditioned inhibitory learning (CI) (Rescorla, 1969;L oL ordo and Fairless, 1985;Hearst, 1988), which occurs when an organism learns that one stimulus (CS) specifically signals the absence of another. A simple and reliable means of producing such noncoincidence learning with vertebrates is the explicitly unpaired procedure (Rescorla and Lolordo, 1965;Wasserman et al., 1974), in which C S and US are both presented during training but are separated by a fixed and relatively long temporal interval. Although a variety of cellular and molecular neural correlates have been reported for behavioral and /or neurophysiological paired-stimulation paradigms, the physiological bases of conditioned inhibitory learning are obscure and unexplored. This neglect of inhibitory learning is surprising, because of the importance of such learning for the behavioral adaptation of organisms. F...

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Section: Discussionmentioning

confidence: 99%

Behavioral and Neural Bases of Noncoincidence Learning inHermissenda

Britton

Farley

1999

J. Neurosci.

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“…If these behaviors were altered, were they altered in a time-speci c way that was consistent with patterns observed in the eld? Natural time-dependent changes in orientation related behaviors have been previously demonstrated in gastropods (Warburton, 1973;Lederhendler et al, 1980). In this case, however, no time-dependent effect of the parasite on the snail's behavior was found.…”

Section: Discussionmentioning

confidence: 44%

“…Differences in the rate of movement in light and dark conditions have been demonstrated in gastropods previously (e.g. Lederhendler et al, 1980).…”

Section: Photokinesismentioning

confidence: 59%

The Effect of a Trematode Parasite (Microphallus Sp.) on the Response of the Freshwater Snail Potamopyrgus Antipodarum to Light and Gravity

Levri¹,

Fisher

2000

Behav

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Parasites often influence the behavior of their hosts in ways that increase the probability of transmission of the parasite. The digenetic trematode Microphallus sp. has been demonstrated to alter the behavior of the New Zealand freshwater snail Potamopyrgus antipodarum in a way that increases the probability that infected snails will be eaten by the final host (waterfowl). Infected snails are found foraging on top of rocks more often in the early morning when waterfowl are feeding and less often in the afternoon when unsuitable hosts (fish) are feeding. The mechanism(s) that the parasite utilizes to produce this behavioral change is not known. The present study investigated three possible behaviors (phototaxis, geotaxis, and photokinesis) that the parasite could alter that may account for the behavioral change seen in the field. Infected and uninfected snails were assessed in terms of their orientation to light (phototaxis), orientation to gravity (geotaxis), and movement in response to light (photokinesis). There was no evidence of phototactic behaviors in either infected or uninfected snails. However, uninfected snails were found to positively orient towards gravity, while infected snails did not. Also, both infected and uninfected snails were found to be positively photokinetic (they move faster in the light than in the dark), but Microphallus infected snails were found to move more slowly than uninfected snails. The differences found between infected and uninfected snails may be part of the manipulative effort of the parasite, but by themselves the differences are not sufficient to explain the patterns observed in the field.

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“…Negative phototaxis is also possible, depending on the light cycle, stimulus intensity, and sensory adaptation. Thus, phototaxis in Hermissenda is inherently a modifiable behavior (Lederhendler, Barnes, & Alkon, 1980).…”

Section: Implicating Causal Relations Between Cellular Function and L...mentioning

confidence: 99%

“…The positive phototactic pattern (typically expressed during the day in response to illumination of moderate intensity) cannot in any way be considered a unitary or reflexive response. A number of measurable components have been described, which includes latency to initiate locomotion (Crow & Offenbach, 1983; Farley & Alkon, 1982; Lederhendler et al, 1980), preferential behavior for particular intensities (Lederhendler et al, 1980), and speed of movement (Farley & Alkon, 1982). More detailed observations of the behavior showed that execution of phototaxis (positive or negative) included responses such as stopping, turning, circling, and side-to-side head movements.…”

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confidence: 99%

Implicating causal relations between cellular function and learning behavior.

Lederhendler¹,

Alkon²

1986

Behavioral Neuroscience

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Learning in the nudibranch mollusc Hermissenda shows many features of vertebrate associative conditioning. Pairings of light and rotation produce conditioned suppression of phototaxis, which is retained for days, shows savings, extinction, contingency sensitivity, and, recently, temporal specificity. In addition, specific features of the behavior have been shown to undergo classical Pavlovian conditioning. Extensive analysis of the neural networks mediating the flow of visual and graviceptive information have demonstrated convergent pathways at specific cellular loci. These cells are critically implicated for a primary role in the conditioned modifications of behavior. A variety of experimental approaches consistently support the proposal that reductions of specific K+ currents in the Type B photoreceptor soma play a causal role for several different behavioral expressions of the conditioning. In this article, we review several of these behaviors to show how the demonstrated close temporal correspondence of cellular and behavioral functions further implicates certain causal relations. For example, studies of the shadow withdrawal behavior of Hermissenda suggest a causal relation between the long-lasting depolarization of the Type B photoreceptor and the animal's reduced ability to turn towards the light at light/dark boundaries. Whereas the shadow response corresponded to cellular events at the end of a light step, responses to the onset of light or rotation were largely unexplored. By using a different approach, we identified behavioral responses during the first few seconds of stimulation with light and rotation. These responses, for which Pavlovian conditioning was demonstrated, correspond closely in time to known cellular correlates.(ABSTRACT TRUNCATED AT 250 WORDS)

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Complex responses to light of the nudibranch Hermissenda crassicornis (Gastropoda: opisthobranchia)

Cited by 19 publications

References 29 publications

Behavioral and Neural Bases of Noncoincidence Learning inHermissenda

Behavioral and Neural Bases of Noncoincidence Learning inHermissenda

The Effect of a Trematode Parasite (Microphallus Sp.) on the Response of the Freshwater Snail Potamopyrgus Antipodarum to Light and Gravity

Implicating causal relations between cellular function and learning behavior.

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