Striatal dopamine integrates cost, benefit and motivation

Eshel, Neir; Touponse, Gavin; Wang, Allan; Osterman, Amber K; Shank, Amei N; Groome, Alexandra M; Taniguchi, Lara; Pinto, Daniel F. Cardozo; Tucciarone, Jason; Bentzley, Brandon S.; Malenka, Robert C.

doi:10.1101/2022.09.20.508777

Cited by 8 publications

(12 citation statements)

References 57 publications

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“…Recent recordings of dopamine release in the striatum using fiber photometry during Restaurant Row have revealed differential signaling patterns of costs coded in the offer zone versus wait zone 62 . Further, dopamine encoded perplexing negative reward-prediction-error-like signals time-locked to volitional change-of-mind quit decisions in the wait zone that could be disrupted optogenetically 62,63 . Altering synaptic strength of glutamatergic inputs into the striatum can also selectively disrupt wait zone behavior without influencing offer zone choices 64 .…”

Section: Discussionmentioning

confidence: 99%

Diabetes alters neuroeconomically dissociable forms of mental accounting

Nwakama,

Durand-de Cuttoli,

Oketokoun

et al. 2024

Preprint

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Those with diabetes mellitus are at high-risk of developing psychiatric disorders, yet the link between hyperglycemia and alterations in motivated behavior has not been explored in detail. We characterized value-based decision-making behavior of a streptozocin-induced diabetic mouse model on a naturalistic neuroeconomic foraging paradigm called Restaurant Row. Mice made self-paced choices while on a limited time-budget accepting or rejecting reward offers as a function of cost (delays cued by tone-pitch) and subjective value (flavors), tested daily in a closed-economy system across months. We found streptozocin-treated mice disproportionately undervalued less-preferred flavors and inverted their meal-consumption patterns shifted toward a more costly strategy that overprioritized high-value rewards. We discovered these foraging behaviors were driven by impairments in multiple decision-making systems, including the ability to deliberate when engaged in conflict and cache the value of the passage of time in the form of sunk costs. Surprisingly, diabetes-induced changes in behavior depended not only on the type of choice being made but also the salience of reward-scarcity in the environment. These findings suggest complex relationships between glycemic regulation and dissociable valuation algorithms underlying unique cognitive heuristics and sensitivity to opportunity costs can disrupt fundamentally distinct computational processes and could give rise to psychiatric vulnerabilities.

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Section: Discussionmentioning

confidence: 99%

Diabetes alters neuroeconomically dissociable forms of mental accounting

Nwakama,

Durand-de Cuttoli,

Oketokoun

et al. 2024

Preprint

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“…This difference in measured evoked concentration may reflect positioning the recording electrode for a maximum signal during implantation in the current study or the greater effectiveness of the transfer when electrical stimulation is used instead of a natural reward. Alternatively, it may reflect differences in motivation—which has been shown to be inversely related to levels of dopamine release (Eshel et al, 2023)—between thirsty rats moving to retrieve a liquid reward and rats receiving sensory stimulation paired with electrical stimulation of their dopamine neurons independent of their behaviour.…”

Section: Discussionmentioning

confidence: 99%

Phasic dopamine signals are reduced in the spontaneously hypertensive rat and increased by methylphenidate

Li,

Huang,

Chen

et al. 2024

Eur J of Neuroscience

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The spontaneously hypertensive rat (SHR) is a selectively bred animal strain that is frequently used to model attention‐deficit hyperactivity disorder (ADHD) because of certain genetically determined behavioural characteristics. To test the hypothesis that the characteristically altered response to positive reinforcement in SHRs may be due to altered phasic dopamine response to reward, we measured phasic dopamine signals in the SHRs and Sprague Dawley (SD) rats using in vivo fast‐scan cyclic voltammetry. The effects of the dopamine reuptake inhibitor, methylphenidate, on these signals were also studied. Phasic dopamine signals during the pairing of a sensory cue with electrical stimulation of midbrain dopamine neurons were significantly smaller in the SHRs than in the SD rats. Over repeated pairings, the dopamine response to the sensory cue increased, whereas the response to the electrical stimulation of dopamine neurons decreased, similarly in both strains. However, the final amplitude of the response to the sensory cue after pairing was significantly smaller in SHRs than in the SD rats. Methylphenidate increased responses to sensory cues to a significantly greater extent in the SHRs than in the SD rats, due largely to differences in the low dose effect. At a higher dose, methylphenidate increased responses to sensory cues and electrical stimulation similarly in SHRs and SD rats. The smaller dopamine responses may explain the reduced salience of reward‐predicting cues previously reported in the SHR, whereas the action of methylphenidate on the cue response suggests a potential mechanism for the therapeutic effects of low‐dose methylphenidate in ADHD.

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“…On each successive trial, the response requirement (lever presses) needed to obtain reward scaled near-logarithmically. The response ratio of the first sixteen trials was: 1, 2, 4, 6,9,12,15,20,25,32,40,50,62,77,95,118. The last response requirement attained, also known as break-point, was recorded and used to infer the inherent motivation for the reward.…”

Section: Methods Detailsmentioning

confidence: 99%

Dynamic Overrepresentation of Accumbal Cues in Food- and Opioid-Seeking Rats after Prenatal THC Exposure

Luján,

Young-Morrison,

Aroni

et al. 2024

Preprint

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The increasing prevalence of cannabis use during pregnancy has raised significant medical concerns, primarily related to the presence of Δ9-tetrahydrocannabinol (THC), which readily crosses the placenta and impacts fetal brain development. Previous research has identified midbrain dopaminergic neuronal alterations related to maternal THC consumption. However, the enduring consequences that prenatal cannabis exposure (PCE) has on striatum-based processing during voluntary reward pursuit have not been specifically determined. Here, we characterize PCE rats during food (palatable pellets) or opioid (remifentanyl)-maintained reward seeking. We find that the supra motivational phenotype of PCE rats is independent of value-based processing and is instead related to augmented reinforcing efficiency of opioid rewards. Our findings reveal that in utero THC exposure leads to increased cue-evoked dopamine release responses and an overrepresentation of cue-aligned, effort-driven striatal patterns of encoding. Recapitulating findings in humans, drug-related neurobiological adaptations of PCE were more pronounced in males, who also showed increased vulnerability for relapse. Collectively, these findings indicate that prenatal THC exposure in male rats engenders to a pronounced neurodevelopmental susceptibility to addiction-like disorders later in life.

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Striatal dopamine integrates cost, benefit and motivation

Cited by 8 publications

References 57 publications

Diabetes alters neuroeconomically dissociable forms of mental accounting

Diabetes alters neuroeconomically dissociable forms of mental accounting

Phasic dopamine signals are reduced in the spontaneously hypertensive rat and increased by methylphenidate

Dynamic Overrepresentation of Accumbal Cues in Food- and Opioid-Seeking Rats after Prenatal THC Exposure

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