Cortical Contributions to Higher-Order Conditioning: A Review of Retrosplenial Cortex Function

In higher-order conditioning paradigms, such as sensory preconditioning or second-order conditioning, discrete (e.g., phasic) or contextual (e.g., static) stimuli can gain the ability to elicit learned responses despite never being directly paired with reinforcement. The purpose of this mini-review is to examine the neuroanatomical basis of high-order conditioning, by selectively reviewing research that has examined the role of the retrosplenial cortex (RSC) in sensory preconditioning and second-order conditioning. For both forms of higher-order conditioning, we first discuss the types of associations that may occur and then review findings from RSC lesion/inactivation experiments. These experiments demonstrate a role for the RSC in sensory preconditioning, suggesting that this cortical region might contribute to higher-order conditioning via the encoding of neutral stimulus-stimulus associations. In addition, we address knowledge gaps, avenues for future research, and consider the contribution of the RSC to higher-order conditioning in relation to related brain structures.

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Higher-Order Conditioning and Dopamine: Charting a Path Forward

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.745388 ◽

2021 ◽

Vol 15 ◽

Author(s):

Benjamin M. Seitz ◽

Aaron P. Blaisdell ◽

Melissa J. Sharpe

Keyword(s):

Causal Reasoning ◽

Higher Order ◽

Second Order ◽

Dopamine Neurons ◽

Sensory Preconditioning ◽

Order Conditioning ◽

Sports Team ◽

Midbrain Dopamine ◽

Complex Forms ◽

Learning And Cognition

Higher-order conditioning involves learning causal links between multiple events, which then allows one to make novel inferences. For example, observing a correlation between two events (e.g., a neighbor wearing a particular sports jersey), later helps one make new predictions based on this knowledge (e.g., the neighbor’s wife’s favorite sports team). This type of learning is important because it allows one to benefit maximally from previous experiences and perform adaptively in complex environments where many things are ambiguous or uncertain. Two procedures in the lab are often used to probe this kind of learning, second-order conditioning (SOC) and sensory preconditioning (SPC). In second-order conditioning (SOC), we first teach subjects that there is a relationship between a stimulus and an outcome (e.g., a tone that predicts food). Then, an additional stimulus is taught to precede the predictive stimulus (e.g., a light leads to the food-predictive tone). In sensory preconditioning (SPC), this order of training is reversed. Specifically, the two neutral stimuli (i.e., light and tone) are first paired together and then the tone is paired separately with food. Interestingly, in both SPC and SOC, humans, rodents, and even insects, and other invertebrates will later predict that both the light and tone are likely to lead to food, even though they only experienced the tone directly paired with food. While these processes are procedurally similar, a wealth of research suggests they are associatively and neurobiologically distinct. However, midbrain dopamine, a neurotransmitter long thought to facilitate basic Pavlovian conditioning in a relatively simplistic manner, appears critical for both SOC and SPC. These findings suggest dopamine may contribute to learning in ways that transcend differences in associative and neurological structure. We discuss how research demonstrating that dopamine is critical to both SOC and SPC places it at the center of more complex forms of cognition (e.g., spatial navigation and causal reasoning). Further, we suggest that these more sophisticated learning procedures, coupled with recent advances in recording and manipulating dopamine neurons, represent a new path forward in understanding dopamine’s contribution to learning and cognition.

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Comparing the magnitudes of second-order conditioning and sensory preconditioning effects

Bulletin of the Psychonomic Society ◽

10.3758/bf03335215 ◽

1991 ◽

Vol 29 (2) ◽

pp. 133-135 ◽

Cited By ~ 5

Author(s):

Robert C. Barnet ◽

Nicholas J. Grahame ◽

Ralph R. Miller

Keyword(s):

Second Order ◽

Sensory Preconditioning ◽

Order Conditioning

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Retrosplenial cortex is necessary for spatial and non-spatial latent learning in mice

10.1101/2021.07.21.453258 ◽

2021 ◽

Author(s):

Ana Carolina Bottura de Barros ◽

Liad J Baruchin ◽

Marios C Panayi ◽

Nils Nyberg ◽

Veronika Samborska ◽

...

Keyword(s):

Decision Making ◽

Brain Area ◽

Brain Structures ◽

Internal Models ◽

Retrosplenial Cortex ◽

Latent Learning ◽

Subjective Value ◽

Spatial Decision Making ◽

The Creation

Latent learning occurs when associations are formed between stimuli in the absence of explicit reinforcement. Traditionally, latent learning in rodents has been associated with the creation internal models of space. However, increasing evidence points to roles of internal models also in non-spatial decision making. Whether the same brain structures and processes support the creation of spatially-anchored or non-spatial internal models via latent learning, is an open question. To address this question, we developed a novel operant box task that allows to test spatial and non-spatial versions of a flavour-based sensory preconditioning paradigm. We probed the role of the retrosplenial cortex, a brain area associated with spatial cognition and subjective value representation, in this task using precise, closed-loop optogenetic silencing during different task phases. We show that the retrosplenial cortex is necessary for both spatial and non-spatial latent learning in mice. We further demonstrate that the requirement of retrosplenial cortex is limited to the preconditioning phase of the task. Our results provide insight into the specific role of the retrosplenial cortex in latent learning, demonstrate that latent learning plays a general part in the creation of internal models, independent of spatial anchors, and provide a novel avenue for studying model-based decision making.

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AUTONOMY AND HIERARCHY

Social Philosophy and Policy ◽

10.1017/s0265052503202065 ◽

2003 ◽

Vol 20 (2) ◽

pp. 156-176 ◽

Cited By ~ 14

Author(s):

Michael E. Bratman

Keyword(s):

Free Will ◽

Higher Order ◽

Second Order ◽

Original Version ◽

Autonomous Action ◽

Original Proposal

In autonomous action the agent herself directs and governs the action. But what is it for the agent herself to direct and to govern? One theme in a series of articles by Harry G. Frankfurt is that we can make progress in answering this question by appeal to higher-order conative attitudes. Frankfurt's original version of this idea is that in acting of one's own free will, one is not acting simply because one desires so to act. Rather, it is also true that this desire motivates one's action because one desires that this desire motivate one's action. This latter desire about the motivational role of one's desire is a second-order desire. It is, in particular, what Frankfurt calls a second-order “volition.” And, according to Frankfurt's original proposal, acting of one's own free will involves in this way such second-order, and sometimes yet higher order, volitions.

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The Opioid Receptor Antagonist Naloxone Enhances First-Order Fear Conditioning, Second-Order Fear Conditioning and Sensory Preconditioning in Rats

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.771767 ◽

2021 ◽

Vol 15 ◽

Author(s):

Robine M. L. Michalscheck ◽

Dana M. Leidl ◽

R. Frederick Westbrook ◽

Nathan M. Holmes

Keyword(s):

Receptor Antagonist ◽

Fear Conditioning ◽

Opioid Receptor ◽

Neutral Stimulus ◽

Second Order ◽

Sensory Preconditioning ◽

First Order ◽

Opioid Receptor Antagonist ◽

Stage 1 ◽

Drug Free

The opioid receptor antagonist naloxone enhances Pavlovian fear conditioning when rats are exposed to pairings of an initially neutral stimulus, such as a tone, and a painful foot shock unconditioned stimulus (US; so-called first-order fear conditioning; Pavlov, 1927). The present series of experiments examined whether naloxone has the same effect when conditioning occurs in the absence of US exposure. In Experiments 1a and 1b, rats were exposed to tone-shock pairings in stage 1 (one trial per day for 4 days) and then to pairings of an initially neutral light with the already conditioned tone in stage 2 (one trial per day for 4 days). Experiment 1a confirmed that this training results in second-order fear of the light; and Experiment 1b showed that naloxone enhances this conditioning: rats injected with naloxone in stage 2 froze more than vehicle-injected controls when tested with the light alone (drug-free). In Experiments 2a and 2b, rats were exposed to light-tone pairings in stage 1 (one trial per day for 4 days) and then to tone-shock pairings in stage 2 (one trial per day for 2 days). Experiment 2a confirmed that this training results in sensory preconditioned fear of the light; and Experiment 2b showed that naloxone enhances sensory preconditioning when injected prior to each of the light-tone pairings: rats injected with naloxone in stage 1 froze more than vehicle-injected controls when tested with the light alone (drug-free). These results were taken to mean that naloxone enhances fear conditioning independently of its effect on US processing; and more generally, that opioids regulate the error-correction mechanisms that underlie associative formation.

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Causal evidence supporting the proposal that dopamine transients function as a temporal difference prediction error

10.1101/520965 ◽

2019 ◽

Cited By ~ 2

Author(s):

Etienne JP Maes ◽

Melissa J Sharpe ◽

Matthew P.H. Gardner ◽

Chun Yun Chang ◽

Geoffrey Schoenbaum ◽

...

Keyword(s):

Prediction Error ◽

Second Order ◽

Prediction Errors ◽

Temporal Difference ◽

Reward Prediction ◽

Order Conditioning ◽

Central Tenet

Reward-evoked dopamine is well-established as a prediction error. However the central tenet of temporal difference accounts – that similar transients evoked by reward-predictive cues also function as errors – remains untested. To address this, we used two phenomena, second-order conditioning and blocking, in order to examine the role of dopamine in prediction error versus reward prediction. We show that optogenetically-shunting dopamine activity at the start of a reward-predicting cue prevents second-order conditioning without affecting blocking. These results support temporal difference accounts by providing causal evidence that cue-evoked dopamine transients function as prediction errors.

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Associations in second-order conditioning and sensory preconditioning.

Journal of Comparative and Physiological Psychology ◽

10.1037/h0033333 ◽

1972 ◽

Vol 81 (1) ◽

pp. 1-11 ◽

Cited By ~ 229

Author(s):

Ross C. Rizley ◽

Robert A. Rescorla

Keyword(s):

Second Order ◽

Sensory Preconditioning ◽

Order Conditioning

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Second-Order Conditioning in Humans

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.672628 ◽

2021 ◽

Vol 15 ◽

Author(s):

Jessica C. Lee

Keyword(s):

Conditioned Inhibition ◽

Large Body ◽

Second Order ◽

Critical Parameters ◽

Future Research ◽

Order Conditioning ◽

Potential Interactions

In contrast to the large body of work demonstrating second-order conditioning (SOC) in non-human animals, the evidence for SOC in humans is scant. In this review, I examine the existing literature and suggest theoretical and procedural explanations for why SOC has been so elusive in humans. In particular, I discuss potential interactions with conditioned inhibition, whether SOC is rational, and propose critical parameters needed to obtain the effect. I conclude that SOC is a real but difficult phenomenon to obtain in humans, and suggest directions for future research.

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