Non‐associative learning in the squid<i>lolliguncula brevis</i>(Mollusca, Cephalopoda)

Long, Tianhang; Hanlon, Roger T.; Maat, A. Ter; Pinsker, H. M.

doi:10.1080/10236248909378736

Cited by 16 publications

(12 citation statements)

References 14 publications

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“…Previous studies using visual stimuli in squid showed a sharp decrease in the number of jetting responses over the first 5 min of exposure but total inhibition of responses was not observed and the squid continued to show a ring pattern when exposed to the fish predator models (Long et al, 1989). Those results are very similar to the results obtained for acoustic habituation in cuttlefish.…”

Section: Research Articlesupporting

confidence: 81%

“…Habituation was noted by a logarithmic decrease in the occurrence of certain responses over the course of 30 exposures (30 min) of repeated 200 Hz tone stimuli. This decrease was notable in the more dramatic escape responses (inking and jetting), and for large body patterning changes; this pattern of habituation is similar to that reported in the squid Lolliguncula brevis (Long et al, 1989). It was significant across both sound levels, suggesting the robustness of this form of habituation.…”

Section: Research Articlesupporting

confidence: 65%

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Graded behavioral responses and habituation to sound in the common cuttlefish, Sepia officinalis

Samson

Mooney

Gussekloo

et al. 2014

Journal of Experimental Biology

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Sound is a widely available and vital cue in aquatic environments, yet most bioacoustic research has focused on marine vertebrates, leaving sound detection in invertebrates poorly understood. Cephalopods are an ecologically key taxon that likely use sound and may be impacted by increasing anthropogenic ocean noise, but little is known regarding their behavioral responses or adaptations to sound stimuli. These experiments identify the acoustic range and levels that elicit a wide range of secondary defense behaviors such as inking, jetting and rapid coloration change. Secondarily, it was found that cuttlefish habituate to certain sound stimuli. The present study examined the behavioral responses of 22 cuttlefish (Sepia officinalis) to pure-tone pips ranging from 80 to 1000 Hz with sound pressure levels of 85-188 dB re. 1 μPa rms and particle accelerations of 0-17.1 m s −2 . Cuttlefish escape responses (inking, jetting) were observed between frequencies of 80 and 300 Hz and at sound levels above 140 dB re. 1 μPa rms and 0.01 m s −2 (0.74 m s −2 for inking responses). Body patterning changes and fin movements were observed at all frequencies and sound levels. Response intensity was dependent upon stimulus amplitude and frequency, suggesting that cuttlefish also possess loudness perception with a maximum sensitivity around 150 Hz. Cuttlefish habituated to repeated 200 Hz tone pips, at two sound intensities. Total response inhibition was not reached, however, and a basal response remained present in most animals. The graded responses provide a loudness sensitivity curve and suggest an ecological function for sound use in cephalopods.

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Section: Research Articlesupporting

confidence: 81%

Section: Research Articlesupporting

confidence: 65%

Graded behavioral responses and habituation to sound in the common cuttlefish, Sepia officinalis

Samson

Mooney

Gussekloo

et al. 2014

Journal of Experimental Biology

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“…For example, the defensive gill and siphon withdrawal response in Aplysia , 40 crab escape response to an overhead shadow, 41 and the squid escape response to visual cues of a predator. 42 Failure to avoid many of the stimuli detected by ASH could be fatal for C. elegans . Why then do reversal responses habituate?…”

Section: Discussionmentioning

confidence: 99%

Habituation as an adaptive shift in response strategy mediated by neuropeptides

Ardiel

Giles

et al. 2017

npj Science Learn

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Habituation is a non-associative form of learning characterized by a decremented response to repeated stimulation. It is typically framed as a process of selective attention, allowing animals to ignore irrelevant stimuli in order to free up limited cognitive resources. However, habituation can also occur to threatening and toxic stimuli, suggesting that habituation may serve other functions. Here we took advantage of a high-throughput Caenorhabditis elegans learning assay to investigate habituation to noxious stimuli. Using real-time computer vision software for automated behavioral tracking and optogenetics for controlled activation of a polymodal nociceptor, ASH, we found that neuropeptides mediated habituation and performed an RNAi screen to identify candidate receptors. Through subsequent mutant analysis and cell-type-specific gene expression, we found that pigmentdispersing factor (PDF) neuropeptides function redundantly to promote habituation via PDFR-1-mediated cAMP signaling in both neurons and muscles. Behavioral analysis during learning acquisition suggests that response habituation and sensitization of locomotion are parts of a shifting behavioral strategy orchestrated by pigment dispersing factor signaling to promote dispersal away from repeated aversive stimuli.

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“…However, in the same organism, massed procedure failed to produce dishabituation (12 tail stimuli, 10-min intervals, with a dishabituatory salt stimulus to the anterior body 2 min before the 11th session (Frost et al 1996). In a cephalopod, the squid Lolliguncula brevis, Long et al (1989) trained animals to inhibit the number of escape jets and the production of a chromatophore ring pattern in response to brief (5-sec) presentations to models of predators. Dishabituation was examined after habituating the squids to a model shark for 15 trials (1-min intervals) and then presenting a threat stimulus (waving a hand near the squid) followed by 15 trials of the same shark presentations.…”

Section: Discussionmentioning

confidence: 99%

“…In cephalopods, the only arousing stimulus previously used was "waving a hand near the squid" (Long et al 1989). We rejected this stimulus on the grounds that it cannot be consistently repeated, and that there is a risk of unintentional cueing.…”

Section: Dishabituation Stimulimentioning

confidence: 99%

The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning?

Agin¹,

Chichery²,

Dickel³

et al. 2006

Learn. Mem.

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This study examines whether or not habituation contributes to the regulation of the inhibition of predatory behavior observed during the "prawn-in-the-tube" training procedure. When presented with prawns that are visible behind glass but untouchable, cuttlefish promptly learn to inhibit their capture attempts. The first three experiments demonstrated that the acquired response in the course of training cannot be dishabituated. The fourth experiment demonstrated that the repeated application of a brief visual prawn stimulus, one that is terminated before the cuttlefish can strike, decreases attack latencies. Taken together, the results of this study establish that habituation does not play a significant role in this learning task. In fact, the present findings strengthen the results of previous studies suggesting that passive avoidance learning contributes to the regulation of the inhibition of predatory behavior.

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Non‐associative learning in the squidlolliguncula brevis(Mollusca, Cephalopoda)

Cited by 16 publications

References 14 publications

Graded behavioral responses and habituation to sound in the common cuttlefish, Sepia officinalis

Graded behavioral responses and habituation to sound in the common cuttlefish, Sepia officinalis

Habituation as an adaptive shift in response strategy mediated by neuropeptides

The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning?

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