Associative Learning in Invertebrates

Hawkins, Robert D.; Byrne, John H.

doi:10.1101/cshperspect.a021709

Cited by 123 publications

(61 citation statements)

References 102 publications

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“…† Maintenance of long-term cellular memory involves both intracellular and extracellular feedback loops, which sustain the regulation of gene expression and the modification of targeted molecules. † As described by Hawkins and Byrne (2015), associative forms of learning and memory can arise from the neural mechanisms that are used for nonassociative learning.…”

Section: Discussionmentioning

confidence: 99%

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Nonassociative Learning in Invertebrates

Byrne¹,

Hawkins

2015

Cold Spring Harb Perspect Biol

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The simplicity and tractability of the neural circuits mediating behaviors in invertebrates have facilitated the cellular/molecular dissection of neural mechanisms underlying learning. The review has a particular focus on the general principles that have emerged from analyses of an example of nonassociative learning, sensitization in the marine mollusk Aplysia. Learning and memory rely on multiple mechanisms of plasticity at multiple sites of the neuronal circuits, with the relative contribution to memory of the different sites varying as a function of the extent of training and time after training. The same intracellular signaling cascades that induce short-term modifications in synaptic transmission can also be used to induce longterm changes. Although short-term memory relies on covalent modifications of preexisting proteins, long-term memory also requires regulated gene transcription and translation. Maintenance of long-term cellular memory involves both intracellular and extracellular feedback loops, which sustain the regulation of gene expression and the modification of targeted molecules.

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Section: Discussionmentioning

confidence: 99%

“…Associative learning includes classical conditioning and operant conditioning, which are discussed by Hawkins and Byrne (2015). Nonassociative forms of learning include habituation and sensitization.…”

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confidence: 99%

Nonassociative Learning in Invertebrates

Byrne¹,

Hawkins

2015

Cold Spring Harb Perspect Biol

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“…In operant conditioning, also referred to as associative learning, an animal also learns to associate certain signals with the positive or negative consequences of their behavior. Operant conditioning has been studied for over a century (Skinner, 2012; Thorndike, 1898), and numerous studies have now contributed to a rich understanding of the environmental and biological factors that underlie animal learning across many species, including invertebrates (Hawkins & Byrne, 2015), birds (Park, Okanoya, & Dooling, 1985), fish (Lucon-Xiccato & Bisazza, 2016; Thompson & Sturm, 1965), and mammals (Grant, 1964), including monkeys (Alvarado, Malkova, & Bachevalier, 2016). …”

Section: Introductionmentioning

confidence: 99%

Effect of reward type on object discrimination learning in socially monogamous coppery titi monkeys (Callicebus cupreus)

Freeman

Rebout

Bales

2018

American J Primatol

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Highly valued food items are often used as rewards to reinforce an animal’s behavior. For social species, social interaction is rewarding and can drive an individual’s behavior as well. In the currently study, we wanted to compare the efficacy of a food reward and a social reward on object discrimination learning in socially monogamous titi monkeys. We hypothesized that titi monkeys would perform more accurately for a social reward (their pair mate) than for a food reward (a highly desired food item). Eleven adult titi monkeys were tested with a two-object visual discrimination task for both types of reward. The colors and shapes of the objects in the two-object discrimination task were counterbalanced across subjects. During each trial, subjects were shown two objects, and the trial ended when the subject touched the reinforced shape (S+) or after 5 min. A correct trial was defined as one when the subject touched S+ first. We found that 45.5% of subjects were able to learn the task with a social reward, and 83.3% were able to learn the task with a food reward. We found that subjects balked more often and had fewer correct trials for the social reward. Finally, subjects took longer to approach the shapes for a social reward, possibly indicating lower motivation to engage in the task when a social reward is used compared to a food reward. Although significantly fewer subjects met criteria of success with the social reward than with the food reward, our results show that titi monkeys can learn a visual discrimination task with either type of reward.

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“…The plasticity of feeding behaviors permit in vivo investigation of associative memory through appetitive and aversive learning paradigms (Hawkins and Byrne, 2015; Nargeot and Simmers, 2011; 2012). We investigated the requirements of calpain protease activity for intermediate and long-term memory formation using an associative operant learning paradigm, learning that food is inedible (LFI).…”

Section: Introductionmentioning

confidence: 99%

Differential role of calpain-dependent protein cleavage in intermediate and long-term operant memory in Aplysia

Lyons

Gardner

Lentsch

et al. 2017

Neurobiology of Learning and Memory

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In addition to protein synthesis, protein degradation or protein cleavage may be necessary for intermediate (ITM) and long-term memory (LTM) to remove molecular constraints, facilitate persistent kinase activity and modulate synaptic plasticity. Calpains, a family of conserved calcium dependent cysteine proteases, modulate synaptic function through protein cleavage. We used the marine mollusk Aplysia californica to investigate the in vivo role of calpains during intermediate and long-term operant memory formation using the learning that food is inedible (LFI) paradigm. A single LFI training session, in which the animal associates a specific netted seaweed with the failure to swallow, generates short (30 min), intermediate (4–6 hr) and long-term (24 hr) memory. Using the calpain inhibitors calpeptin and MDL-28170, we found that ITM requires calpain activity for induction and consolidation similar to the previously reported requirements for persistent protein kinase C activity in intermediate-term LFI memory. The induction of LTM also required calpain activity. In contrast to ITM, calpain activity was not necessary for the molecular consolidation of LTM. Surprisingly, six hours after LFI training we found that calpain activity was necessary for LTM, although this is a time at which neither persistent PKC activity nor protein synthesis is required for the maintenance of long-term LFI memory. These results demonstrate that calpains function in multiple roles in vivo during associative memory formation.

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Associative Learning in Invertebrates

Cited by 123 publications

References 102 publications

Nonassociative Learning in Invertebrates

Nonassociative Learning in Invertebrates

Effect of reward type on object discrimination learning in socially monogamous coppery titi monkeys (Callicebus cupreus)

Differential role of calpain-dependent protein cleavage in intermediate and long-term operant memory in Aplysia

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