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Deciphering Decision Making: Variation in Animal Models of Effort- and Uncertainty-Based Choice Reveals Distinct Neural Circuitries Underlying Core Cognitive Processes

Catharine A. Winstanley and Stan B. Floresco
Journal of Neuroscience 30 November 2016, 36 (48) 12069-12079; DOI: https://doi.org/10.1523/JNEUROSCI.1713-16.2016
Catharine A. Winstanley
Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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Stan B. Floresco
Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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    Figure 1.

    Two assays used to probe decision-making involving uncertainty that use different magnitudes of rewards and distinct punishments. A, In the RDT, rats are trained to choose between two levers that delivers either 1 pellet (Small/Safe lever) or 4 pellets (Large/Risky lever), both of which are delivered with 100% certainty. However, selection of the Risky Lever may also deliver a foot shock punisher, and the probability of punishment increases over blocks of trials within a session. B, The rGT was patterned after the IGT used with human subjects. In each 30 min session, rats try to maximize sugar pellet profits by choosing between four options that vary in the number of sugar pellets (1–4) that can be earned on win trials, but also the probability (0.1–0.6) and duration (5–40 s) of punishing time-out periods delivered on losses. “Safe” options associated with smaller per-trial gains yield the most reward per session, whereas “risky” options appear tempting due to the larger reward size but result in less reward over time due to the longer and more frequent time-out punishments they are paired with. In the cued rGT, delivery of reward is accompanied by a 2 s audiovisual cue that increases in complexity with the reward size.

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    Figure 2.

    A comparison of the effects of BLA lesions/inactivation on three forms of decision-making involving uncertainty. A, On the rGT (see Fig. 1B), subjects choose between options that vary in terms of the probability of obtaining different magnitudes of reward associated with different durations of time-out punishments, with some options being more advantageous (“better”) in the long term. BLA lesions cause disadvantageous patterns of decision making, with rats selecting options that yield larger but less frequent rewards and receiving more time-outs. Adapted with permission from Zeeb and Winstanley (2011). B, In the RDT (see Fig. 1A), rats choose between smaller rewards and larger ones associated with increasing likelihood of foot shock punishment. Again, BLA lesions increase choice of the risky option, such that rats receive more foot shocks, as well as more reward. Adapted with permission from Orsini et al. (2015a). C, In contrast, the PDT entails choice between a small/certain reward and a larger, uncertain one, with the probability of receiving the large reward varying across blocks of trials within a session. Unlike the rGT or RDT, there are no explicit punishments associated with the uncertain reward. Here, BLA inactivations reduce choice of larger, uncertain rewards, most prominently when the uncertain option is of equal or greater utility relative to the certain one. Adapted with permission from Ghods-Sharifi et al. (2009).

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    Figure 3.

    A comparison of the effects of lateral OFC inactivation on two forms of decision making involving uncertainty. A, On a given trial of the Betting task, the number of pellets available on the certain lever (or “bet size”) are signaled by illumination of an equivalent number of cue lights on the opposite wall. A nosepoke at each illuminated aperture turns off the light inside. When all the lights have been extinguished in this way, the two levers are presented. Choice of the certain option results in guaranteed delivery of the bet size, whereas a response on the uncertain lever leads to double that amount or nothing with 50:50 odds. As such, there is no net advantage, with respect to pellets earned, in choosing one option over another: even though the bet size shifts across blocks of 10 trials between 1 and 3 sugar pellets, the relative utility of each option remains equal and constant. B, In the PDT, rats choose between a small/certain reward and larger reward delivered with varying probabilities. In contrast to the betting task, the utility of the two options differs and changes across trial blocks. C, Under control conditions on the rBT, some animals show sensitivity to bet size (wager sensitive, left), and decrease preference for the uncertain option when greater amounts of reward are at stake. Other rats are relatively wager insensitive (right). OFC inactivation increased choice of the uncertain option in wager-sensitive rats when bet sizes were large while having no effect on wager-insensitive rats. D, In contrast to the rBT, OFC inactivation does not affect choice behavior on the PDT. A comparison of these two observations suggests that the OFC may play a more prominent role in directing risk-related decisions influenced by subjective biases, independent of reward utility.

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    Table 1.

    Relationship between task features and neurobiology implicated in decision-making assays involving an assessment of uncertaintya

    Task typeTask feature presentNeurobiology implicated in risky choice
    LossContingency shiftUtility matchedBLAlOFCmPFCDA
    rIGT✓Embedded ImageEmbedded Image?—b??
    rGT✓Embedded ImageEmbedded Image↑—↓Embedded Imagec
    RDT✓✓Embedded Image↑↓?✓
    PDTEmbedded Image✓Embedded Image↓—↑↓d✓
    rBTEmbedded Image✓✓—↑—✓
    • ↵a Symbols are used to indicate whether risky choice is increased (↑), decreased (↓), or unaffected (—) by inactivation or silencing of the BLA, lateral OFC, or regions of the mPFC. The last column provides a somewhat crude overview of whether DA plays a strong role in mediating choice, based on the effects of acute or chronic pharmacological challenges with specific dopaminergic agents (i.e., not just psychostimulants, which can act on a multitude of neurochemical signaling systems).

    • ↵b This is inferred from cFos staining, rather than inactivation/lesion experiments.

    • ↵c The cued version of the rGT is sensitive to D3 receptor agonists and antagonists.

    • ↵d The presence of both upward and downward arrows signifies that risky choice can be both increased and decreased by targeting different DA receptor subtypes, particularly in frontal cortex, such that a simple linear relationship between DA tone and risky choice is unlikely.

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    Table 2.

    Relationship between task features and neurobiology implicated in different decision-making assays involving the assessment of efforta

    Task typeType of effort taxedNeurobiology implicated in risky choice
    Type of effortEffortful challengeNAcBLAACCmPFCDA
    T-mazePhysicalComplete one unique and effortful action (scale barrier)↓↓↓—✓
    Concurrent choice taskPhysicalComplete more units of equally effortful response (lever press) versus none↓NA——✓
    EDTPhysicalComplete more units of equally effortful response (lever press) versus less↓↓——✓
    rCETCognitiveAccurately localize brief visual stimulus (attentionally demanding)—b↑↓↓↓Embedded Image
    • ↵a Symbols are used to indicate whether choice of the effortful option is increased (↑), decreased (↓), or unaffected (—) by inactivation or silencing of the NAc, BLA, ACC, or regions of the mPFC. The last column provides a rough indication of whether DA plays a strong role in mediating choice, based on the effects of acute or chronic pharmacological challenges with specific dopaminergic agents.

    • ↵b NAC inactivation completely abolished performance of the rCET task; therefore, it is impossible to conclude that a selective reduction in choice of the harder option is observed, although obviously such choice does decline.

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The Journal of Neuroscience: 36 (48)
Journal of Neuroscience
Vol. 36, Issue 48
30 Nov 2016
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Deciphering Decision Making: Variation in Animal Models of Effort- and Uncertainty-Based Choice Reveals Distinct Neural Circuitries Underlying Core Cognitive Processes
Catharine A. Winstanley, Stan B. Floresco
Journal of Neuroscience 30 November 2016, 36 (48) 12069-12079; DOI: 10.1523/JNEUROSCI.1713-16.2016

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Deciphering Decision Making: Variation in Animal Models of Effort- and Uncertainty-Based Choice Reveals Distinct Neural Circuitries Underlying Core Cognitive Processes
Catharine A. Winstanley, Stan B. Floresco
Journal of Neuroscience 30 November 2016, 36 (48) 12069-12079; DOI: 10.1523/JNEUROSCI.1713-16.2016
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