Neurobiological changes in striatal glutamate are associated with trait impulsivity of differential reinforcement of low-rate-response behavior in male rats

Chuang, Chuen-Yu; Tsai, Shau‐Wei; Chen, Shuo-Fu; Yang, Yihua; Chao, Chih-Chang; Yen, Nai-Shing; Liao, Ruey-Ming

doi:10.1016/j.nlm.2020.107352

Cited by 7 publications

(13 citation statements)

References 46 publications

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“…While plentiful evidence supported response inhibition or interval timing, some have suggested that it might be both behaviours, not just one of them, underlying the DRL 26,29,[33][34][35][36] . For example, in our previous experiment, as the rats' efficiency ratio increased from the 7th to the 14th day, we found an increasing peak time to the criterion time interval, but also a decreasing burst responses in high-impulsive rats 30 . However, whether both behaviours modulated the DRL simultaneously or alternatively on different processes or by different orders has remained unknown.…”

Section: Interval Timing Relative To Response Inhibition In the Diffe...mentioning

confidence: 53%

“…After the maximum of the summed pressing responses of a four-second epoch was identified, the peak time was the average value in ms of all IRTs that fell within those four bins (i.e. the maximal epoch), which showed the time point where participants pressed the button with the highest numbers, reflecting their expected criterion time in DRL 30 , 81 . In SSRT, the false-responding rate from only stop-signal trials, namely the percentage of false-pressing reactions, was calculated as the index of response disinhibition.…”

Section: Methodsmentioning

confidence: 99%

“…This type of responding, defined as the burst responses, is usually observed in large quantities as the first peak on a bimodal IRT distribution from the previous DRL results [25][26][27] . For example, the high-impulsive rats being either selected by the lower efficiency ratio behaviourally or induced by the injection of d-amphetamine or cocaine were found to have a higher number of burst responses than that of the low-impulsive rats on distinctive interval-timing DRL schedules [28][29][30] . The burst responses hence has been considered a prominent index of heightened impulsivity, and even loss of self-control in the DRL behaviour 29,[31][32][33] .…”

Section: Interval Timing Relative To Response Inhibition In the Diffe...mentioning

confidence: 99%

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Interval timing relative to response inhibition in the differential reinforcement of low-rate responding in normally developing young adults

Yang¹,

Liao²,

Su³

et al. 2023

Sci Rep

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With recent proposal suggesting the multifaceted nature of impulsivity, researchers have been intrigued by the question of whether the impulsive behaviour measured in the traditionally psychological paradigms is unitary. One such paradigm, the differential reinforcement of low-rate responding (DRL), has been used to assess response inhibition, but its underlying mechanism has still been debated. In present research, we examined and differentiated the effects of both response inhibition and interval timing on a multisession DRL-10 s (DRL-10 s) in a large sample of normally developing young adults, as well as with three other measures including the stop-signal reaction task (SSRT), time production task-10 s (TPT-10 s), and the Barrett impulsivity scale-11 (BIS-11). The results showed that behavioural changes existed in DRL. As the task sessions progressed, there was an increase in both reinforcement probability and peak time, but a decrease in burst responses. Most importantly, both principal component analysis and generalized multilevel modeling yielded consistent results that as the task progressed, there was an increasing involvement of the TPT in the late sessions of DRL. However, none of the effect of SSRT was found. In sum, the differential degrees of involvement of the timing process, relative to response inhibition, were observed in DRL.

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Section: Interval Timing Relative To Response Inhibition In the Diffe...mentioning

confidence: 53%

Section: Methodsmentioning

confidence: 99%

Section: Interval Timing Relative To Response Inhibition In the Diffe...mentioning

confidence: 99%

See 1 more Smart Citation

Interval timing relative to response inhibition in the differential reinforcement of low-rate responding in normally developing young adults

Yang¹,

Liao²,

Su³

et al. 2023

Sci Rep

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“…Here, we expanded upon these prior findings by presenting new insights into the neural circuit underlying motor impulsivity, highlighting the significant contribution of mPFC neurons projecting to the NAc. The cortical neurons projecting to the NAc are mainly glutamatergic and, interestingly, high impulsive animals display lower glutamate in the NAc compared to low impulsive rats 56 , suggesting that disrupted glutamatergic transmission between mPFC and NAc is involved, at least partly, for high impulsive behaviors.…”

Section: Discussionmentioning

confidence: 99%

Activation of the mPFC-NAc pathway reduces motor impulsivity but does not affect risk-related decision-making in innately high-impulsive rats

Arrondeau,

Urueña-Méndez,

Marchessaux

et al. 2024

Preprint

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Attention-deficit/hyperactivity disorder (ADHD) and substance use disorders (SUD) are characterized by exacerbated motor and risk-related impulsivities, which are associated with decreased cortical activity. In rodents, the medial prefrontal cortex (mPFC) and nucleus accumbens (NAc) have been separately implicated in impulsive behaviors, but studies on the specific role of the mPFC-NAc pathway in these behaviors are limited. Here, we investigated whether heightened impulsive behaviors are associated with reduced mPFC activity in rodents, and determined the involvement of the mPFC-NAc pathway in motor and risk-related impulsivities. We used the Roman High- (RHA) and Low-Avoidance (RLA) rat lines, which display divergent phenotypes in impulsivity. To investigate alterations in cortical activity in relation to impulsivity, regional brain glucose metabolism was measured using positron emission tomography and [18F]-fluorodeoxyglucose ([18F]FDG). Using chemogenetics, the activity of the mPFC-NAc pathway was either selectively activated in high-impulsive RHA rats or inhibited in low-impulsive RLA rats, and the effects of these manipulations on motor and risk-related impulsivity were concurrently assessed using the rat gambling task. We showed that basal [18F]FDG uptake was lower in the mPFC and NAc of RHA compared to RLA rats. Activation of the mPFC-NAc pathway in RHA rats reduced motor impulsivity, without affecting risk-related decision-making. Conversely, inhibition of the mPFC-NAc pathway had no effect in RLA rats. Our results suggest that the mPFC-NAc pathway controls motor impulsivity, but has limited involvement in risk-related decision-making. Our findings suggest that reducing fronto-striatal activity may help attenuate motor impulsivity in patients with impulse control dysregulation like ADHD or SUD.

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“…Velazquez-Sanchez et al (2014) applied a DRL 15-s task to select highand low-impulsive rats and reported a food 'addiction' phenotype in high-impulsive subjects. More recently, Chuang et al (2021) used a DRL 10-s task to divide a cohort of rats into high-, medium-, and low-impulsive subgroups. By using in vivo non-invasive proton magnetic resonance spectroscopy ( 1 H-MRS), this study was the first to show that the high-impulsive group had a lower glutamate level in the NA compared to the low-impulsive group.…”

Section: Future Directions and Potentials Of Using The Drl Taskmentioning

confidence: 99%

Investigating Temporal Memory Strength and Time-Based Impulse Control Using the DRL Task

Cheng

Liao

2022

Timing Time Percept.

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Differential reinforcement of low rate (DRL) responding is a schedule-controlled behavior sometimes used in timing research, but also received critics of not providing a pure measure of timing due to the influence of the subject’s motivation or inhibitory control. Nevertheless, we argue that the DRL task provides a unique approach to study how timing and emotion interact with each other. Here, we review evidence showing that male rats prenatally treated with choline supplementation had difficulty in acquiring longer criterion times in the DRL task. This was possibly due to the stronger memory strength of their previously learned shorter criterion times. Female rats, in contrast, performed better than male rats in the same task, but those receiving prenatal choline supplementation were the best performers in this task with longer criterion times because they required less training. Like all female rats, male rats treated with prenatal choline supplementation made very few burst responses, suggesting that the treatment improved male rats’ emotional regulation when facing ‘frustrating’ outcomes. The differential impulse control plus different memory strength of the rats trained in the DRL task revealed the potential interaction of sex hormones and prenatal choline supplementation, a rare combination in a single animal study on timing and time perception. In summary, although the DRL task is certainly not the best timing task, it may be useful in assisting us in better understanding how time perception participates in emotional regulation, especially relevant when the emotion is triggered by a failure in timing.

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Neurobiological changes in striatal glutamate are associated with trait impulsivity of differential reinforcement of low-rate-response behavior in male rats

Cited by 7 publications

References 46 publications

Interval timing relative to response inhibition in the differential reinforcement of low-rate responding in normally developing young adults

Interval timing relative to response inhibition in the differential reinforcement of low-rate responding in normally developing young adults

Activation of the mPFC-NAc pathway reduces motor impulsivity but does not affect risk-related decision-making in innately high-impulsive rats

Investigating Temporal Memory Strength and Time-Based Impulse Control Using the DRL Task

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