The three principles of action: a Pavlovian-instrumental transfer hypothesis

Cartoni, Emilio; Puglisi-Allegra, Stefano; Baldassarre, Gianluca

doi:10.3389/fnbeh.2013.00153

Cited by 47 publications

(47 citation statements)

References 28 publications

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“…This is supported by the fact that responding was elevated even during the first pre-CS interval, before any cue presentation. This interpretation is consistent with a recent theoretical model of PIT put forth by Cartoni et al (2013), which argues that behavioral inhibition is in fact necessary for specific PIT since responding is not affected by a cue that has been paired with a different action and reward. Our findings add to this model that behavioral inhibition is necessary not only in the presence of unpaired cues (the basis for specific PIT), but also at baseline within the reward-associated context.…”

supporting

confidence: 91%

“…IlPFC sends a dense glutamatergic projection to NAcS, a structure that is itself necessary for specific PIT (Corbit and Balleine 2011), and this projection is known to inhibit inappropriate reward seeking (Vertes 2004;Peters et al 2008Peters et al , 2009Bossert et al 2012). Such behavioral inhibition may also be an important element of specific PIT, as responding is not invigorated by a cue that has been paired with a different reward and response (Cartoni et al 2013). …”

mentioning

confidence: 99%

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Infralimbic prefrontal cortex interacts with nucleus accumbens shell to unmask expression of outcome-selective Pavlovian-to-instrumental transfer

Keistler

Barker²,

Taylor

2015

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Although several studies have examined the subcortical circuitry underlying Pavlovian-to-instrumental transfer (PIT), the role of medial prefrontal cortex in this behavior is largely unknown. Elucidating the cortical contributions to PIT will be key for understanding how reward-paired cues control behavior in both adaptive and maladaptive context (i.e., addiction). Here we use bilateral lesions in a rat model to show that infralimbic prefrontal cortex (ilPFC) is necessary for appropriate expression of PIT. Further, we show that ilPFC mediates this effect via functional connectivity with nucleus accumbens shell (NAcS). Together, these data provide the first demonstration that a specific cortico-striatal circuit is necessary for cue-invigorated reward seeking during specific PIT.Cue-motivated reward seeking often requires integration of instrumental response-outcome (R-O) associations with Pavlovian stimulus-outcome (S-O) associations (Rescorla 1990). Experimentally, this integration can be assessed using the Pavlovian-to-instrumental transfer (PIT) task, which measures the ability of reward-associated stimuli to invigorate instrumental responding, even when the R-O and S -O associations have been acquired independently (Estes 1948;Rescorla and Solomon 1967;Lovibond 1983). PIT tasks can be structured to test the generalized arousing effects of Pavlovian cues on behavior (i.e., general PIT) or to test the transfer of Pavlovian information about a specific reward onto the precise behavior that produces that reward (i.e., specific PIT) (Balleine and Ostlund 2007;Holmes et al. 2010). A growing body of work suggests that the specific form of PIT depends on distinct neural substrates, including the basolateral amygdala (BLA) and nucleus accumbens shell (NAcS) Balleine 2005, 2011). However, in contrast to amygdalo-striatal circuitry, the role of medial prefrontal cortex (mPFC) in these behaviors is unknown. The mPFC integrates affective information and instrumental output to attribute incentive value to stimuli, and is therefore well situated to play a key role in cue-guided behavior (Christakou et al. 2004;Homayoun and Moghaddam 2009). While dorsal regions of mPFC-anterior cingulate cortex (ACC) and prelimbic cortex (plPFC)-are not required for PIT (Cardinal et al. 2003;Corbit and Balleine 2003), a role for the more ventral infralimbic cortex (ilPFC) has not been investigated. IlPFC regulates flexible reward seeking and may facilitate cuecontrolled behavior (Barker et al. 2014). IlPFC sends a dense glutamatergic projection to NAcS, a structure that is itself necessary for specific PIT (Corbit and Balleine 2011), and this projection is known to inhibit inappropriate reward seeking (Vertes 2004;Peters et al. 2008Peters et al. , 2009Bossert et al. 2012). Such behavioral inhibition may also be an important element of specific PIT, as responding is not invigorated by a cue that has been paired with a different reward and response (Cartoni et al. 2013).We therefore hypothesized that ilPFC and its projection to the NAcS are r...

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supporting

confidence: 91%

mentioning

confidence: 99%

Infralimbic prefrontal cortex interacts with nucleus accumbens shell to unmask expression of outcome-selective Pavlovian-to-instrumental transfer

Keistler

Barker²,

Taylor

2015

Learn. Mem.

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“…The invigoration of instrumental activity induced by the sucrose-predictive cue could be interpreted to reflect primarily the general (rather than specific) form PIT, because the stimulus invigorated responding on an action that, in training, earned a distinct, grape-flavored polycose reward (Dickinson & Balleine 2002, Cartoni et al 2013, Fanselow & Wassum 2015, Balleine 1994, Dickinson & Balleine 1994). Indeed, sucrose and polycose work through separate taste channels in the rat (Sclafani 1991, Ackroff et al 1993) and were confirmed here to be discriminable.…”

Section: Discussionmentioning

confidence: 99%

Nucleus accumbens core dopamine signaling tracks the need‐based motivational value of food‐paired cues

Aitken¹,

Greenfield²,

Wassum³

2016

Journal of Neurochemistry

104

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Environmental reward-predictive stimuli provide a major source of motivation for instrumental reward-seeking activity and this has been linked to dopamine signaling in the nucleus accumbens (NAc). This cue-induced incentive motivation can be quite general, not restricted to instrumental actions that earn the same unique reward, and is also typically regulated by one’s current need state, such that cues only motivate actions when this is adaptive. But it is unknown whether cue-evoked dopamine signaling is similarly regulated by need state. Here we used fast-scan cyclic voltammetry to monitor dopamine concentration changes in the NAc core of rats during a Pavlovian-to-instrumental transfer (PIT) task in which the motivating influence of two cues, each signaling a distinct food reward (sucrose or food pellets), over an action earning a third unique food reward (grape-flavored polycose) was assessed in a state of hunger and of satiety. Both cues elicited a robust NAc dopamine response when hungry. The magnitude of the sucrose cue-evoked dopamine response correlated with the PIT effect that was selectively induced by this stimulus. Satiety attenuated these cue-evoked dopamine responses and behavioral responding, even though rats had never experienced the specific food rewards in this state. These data demonstrate that cue-evoked NAc core responses are sensitive to current need state, one critical variable that determines the current adaptive utility of cue-motivated behavior.

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“…In the end, this PIT paradigm allowed us to look at the force ratio between hands as a measure for the so-called “specific PIT” and at the time spent inside the target meaning how long they held the cursor at the required target force level or above as a measure for “general PIT”. A specific PIT is when a Pavlovian stimulus associated with a particular outcome selectively enhances the instrumental responding associated with that specific outcome (Corbit and Balleine, 2005; Cartoni et al, 2013). For example, participants squeeze more with their dominant hand when they observe the Pavlovian stimulus because both the stimulus and response have been paired with the monetary reward previously (i.e., via stimulus-outcome-response contingency).…”

Section: Methodsmentioning

confidence: 99%

Monetary, Food, and Social Rewards Induce Similar Pavlovian-to-Instrumental Transfer Effects

Lehner

Balsters²,

Herger³

et al. 2017

Front. Behav. Neurosci.

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Multiple types of reward, such as money, food or social approval, are capable of driving behavior. However, most previous investigations have only focused on one of these reward classes in isolation, as such it is not clear whether different reward classes have a unique influence on instrumental responding or whether the subjective value of the reward, rather than the reward type per se, is most important in driving behavior. Here, we investigate behavior using a well-established reward paradigm, Pavlovian-to-instrumental transfer (PIT), and three different reward types: monetary, food and social rewards. The subjective value of each reward type was matched using a modified Becker-DeGroot-Marschak (BDM) auction where subjective reward value was expressed through physical effort using a bimanual grip force task. We measured the influence of reward-associated stimuli on how participants distributed forces between hands when reaching a target effort range on the screen bimanually and on how much time participants spent in this target range. Participants spent significantly more time in the target range (15% ± 2% maximal voluntary contraction) when a stimulus was presented that was associated with a reward used during instrumental conditioning or Pavlovian conditioning compared to a stimulus associated with a neutral outcome (i.e., general PIT). The strength of the PIT effect was modulated by subjective value (i.e., individuals who showed a stronger PIT effect rated the value of rewards more highly), but not by reward type, demonstrating that stimuli of all reward types were able to act as appetitive reinforcers and influenced instrumental responding, when matched to the same subjective reward value. This is the first demonstration that individually matched monetary, food and social rewards are equally effective as appetitive reinforcers in PIT. These findings strengthen the hypotheses that the subjective value is crucial for how much reward-associated stimuli influence behavior.

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The three principles of action: a Pavlovian-instrumental transfer hypothesis

Cited by 47 publications

References 28 publications

Infralimbic prefrontal cortex interacts with nucleus accumbens shell to unmask expression of outcome-selective Pavlovian-to-instrumental transfer

Infralimbic prefrontal cortex interacts with nucleus accumbens shell to unmask expression of outcome-selective Pavlovian-to-instrumental transfer

Nucleus accumbens core dopamine signaling tracks the need‐based motivational value of food‐paired cues

Monetary, Food, and Social Rewards Induce Similar Pavlovian-to-Instrumental Transfer Effects

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