Transient inactivation of the pigeon hippocampus or the nidopallium caudolaterale during extinction learning impairs extinction retrieval in an appetitive conditioning paradigm

Lengersdorf, Daniel; Stüttgen, Maik C.; Uengoer, Metin; Güntürkün, Onur

doi:10.1016/j.bbr.2014.02.025

Cited by 30 publications

(32 citation statements)

References 60 publications

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“…The hippocampus mediates object-context information processing both in humans (Sadeh et al, 2012 ) and rodents (Goh and Manahan-Vaughan, 2013a , b ). It is likely that the hippocampus mediates both context-specific components to learning about the relationship of the CS and the US and may mediate context-dependent extinction learning and renewal (Corcoran et al, 2005 ; Ji and Maren, 2005 , 2008 ; Koseki et al, 2009 ; Fujiwara et al, 2012 ; Lengersdorf et al, 2014 ; Wiescholleck et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

The metabotropic glutamate receptor, mGlu5, is required for extinction learning that occurs in the absence of a context change

2014

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The metabotropic glutamate (mGlu) receptors and, in particular, mGlu5 are crucially involved in multiple forms of synaptic plasticity that are believed to underlie explicit memory. MGlu5 is also required for information transfer through neuronal oscillations and for spatial memory. Furthermore, mGlu5 is involved in extinction of implicit forms of learning. This places this receptor in a unique position with regard to information encoding. Here, we explored the role of this receptor in context-dependent extinction learning under constant, or changed, contextual conditions. Animals were trained over 3 days to take a left turn under 25% reward probability in a T-maze with a distinct floor pattern (Context A). On Day 4, they experienced either a floor pattern change (Context B) or the same floor pattern (Context A) in the absence of reward. After acquisition of the task, the animals were returned to the maze once more on Day 5 (Context A, no reward). Treatment with the mGlu5 antagonist, 2-methyl-6-(phenylethynyl) pyridine, before maze exposure on Day 4 completely inhibited extinction learning in the AAA paradigm but had no effect in the ABA paradigm. A subsequent return to the original context (A, on Day 5) revealed successful extinction in the AAA paradigm, but impairment of extinction in the ABA paradigm. These data support that although extinction learning in a new context is unaffected by mGlu5 antagonism, extinction of the consolidated context is impaired. This suggests that mGlu5 is intrinsically involved in enabling learning that once-relevant information is no longer valid. © 2014 The Authors. Hippocampus Published by Wiley Periodicals, Inc.

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Section: Introductionmentioning

confidence: 99%

The metabotropic glutamate receptor, mGlu5, is required for extinction learning that occurs in the absence of a context change

2014

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“…Thus, these neurons seem to convey a motor plan for the execution of leftwards or rightwards head movements, rather than representing stimulus luminance. The interpretation that these neurons are involved in action planning resonates well with several previous results: (i) temporary blockade of N ‐methyl‐D‐aspartate receptors in the NCL results in impaired response selection in matching‐to‐sample tasks (Lissek & Güntürkün, , ), (ii) transient inactivation of the NCL through tetrodotoxin leads to an overall suppression of operant behavior (Lengersdorf et al ., ) and (iii) impairs the execution of learned action sequences, leading to both action omission and action perseveration without impairment of visuomotor performance (Helduser & Güntürkün, ).…”

Section: Discussionmentioning

confidence: 99%

Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions

Lengersdorf¹,

Pusch²,

Güntürkün³

et al. 2014

Eur J of Neuroscience

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Sensory systems provide organisms with information on the current status of the environment, thus enabling adaptive behavior. The neural mechanisms by which sensory information is exploited for action selection are typically studied with mammalian subjects performing perceptual decision-making tasks, and most of what is known about these mechanisms at the single-neuron level is derived from cortical recordings in behaving monkeys. To explore the generality of neural mechanisms underlying perceptual decision making across species, we recorded single-neuron activity in the pigeon nidopallium caudolaterale (NCL), a non-laminated associative forebrain structure thought to be functionally equivalent to mammalian prefrontal cortex, while subjects performed a visual categorisation task. We found that, whereas the majority of NCL neurons unspecifically upregulated or downregulated activity during stimulus presentation, ~20% of neurons exhibited differential activity for the sample stimuli and predicted upcoming choices. Moreover, neural activity in these neurons was ramping up during stimulus presentation and remained elevated until a choice was initiated, a response pattern similar to that found in monkey prefrontal and parietal cortices in saccadic choice tasks. In addition, many NCL neurons coded for movement direction during choice execution and differentiated between choice outcomes (reward and punishment). Taken together, our results implicate the NCL in the selection and execution of operant responses, an interpretation resonating well with the results of previous lesion studies. The resemblance of the response patterns of NCL neurons to those observed in mammalian cortex suggests that, despite differing neural architectures, mechanisms for perceptual decision making are similar across classes of vertebrates.

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“…Once a purposeful behavior is acquired, the ability to extinguish it as a result of altered reward contingencies is also essential for survival. The importance of this so-called extinction learning is emphasized by the fact that all vertebrate and invertebrate species tested exhibit this ability (7)(8)(9)(10)(11)(12)(13)(14) .…”

Section: Introductionmentioning

confidence: 99%

Emergence of complex dynamics of choice due to repeated exposures to extinction learning

Donoso

Packheiser

Pusch

et al. 2020

Preprint

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Extinction learning, the process of ceasing an acquired behavior in response to altered reinforcement contingencies, is essential for survival in a changing environment. So far, research has mostly neglected the learning dynamics and variability of behavior during extinction learning and instead focused on a few response types that were studied by population averages. Here, we take a different approach by analyzing the trial-by-trial dynamics of operant extinction learning in both pigeons and a computational model. The task involved discriminant operant conditioning in context A, extinction in context B, and a return to context A to test the context-dependent return of the conditioned response (ABA renewal). By studying single learning curves across animals under repeated sessions of this paradigm, we uncovered a rich variability of behavior during extinction learning: (1) Pigeons prefer the unrewarded alternative choice in one-third of the sessions, predominantly during the very first extinction session an animal encountered. (2) In later sessions, abrupt transitions of behavior at the onset of context B emerge, and (3) the renewal effect decays as sessions progress. While these results could be interpreted in terms of rule learning mechanisms, we show that they can be parsimoniously accounted for by a computational model based only on associative learning between stimuli and actions. Our work thus demonstrates the critical importance of studying the trial-by-trial dynamics of learning in individual sessions, and the unexpected power of "simple" associative learning processes. Significance StatementOperant conditioning is essential for the discovery of purposeful actions, but once a stimulus-response association is acquired, the ability to extinguish it in response to altered reward contingencies is equally important. These processes also play a fundamental role in the development and treatment of pathological behaviors such as drug addiction, overeating and gambling. Here we show that extinction learning is not limited to the cessation of a previously reinforced response, but also drives the emergence of complex and variable choices that change from learning session to learning session. At first sight, these behavioral changes appear to reflect abstract rule learning, but we show in a computational model that they can emerge from "simple" associative learning.

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Transient inactivation of the pigeon hippocampus or the nidopallium caudolaterale during extinction learning impairs extinction retrieval in an appetitive conditioning paradigm

Cited by 30 publications

References 60 publications

The metabotropic glutamate receptor, mGlu5, is required for extinction learning that occurs in the absence of a context change

The metabotropic glutamate receptor, mGlu5, is required for extinction learning that occurs in the absence of a context change

Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions

Emergence of complex dynamics of choice due to repeated exposures to extinction learning

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