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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 64  |  Issue : 5  |  Page : 218-224

Does positive feeling lead to more impulsiveness? – Implication of previous rewarded experience on location-dependent motoric impulsivity


1 Department of Physiology, National Defense Medical Center, Taipei, Taiwan
2 Department of Psychiatry, Hualien Armed Forces General Hospital, Hualien, Taiwan
3 Department of Physiology, Laboratory of Cognitive Neuroscience, National Defense Medical Center, Taipei, Taiwan
4 Genomics Research Center, Academia Sinica, Taipei, Taiwan
5 Department of Physiology, Laboratory of Cognitive Neuroscience, National Defense Medical Center; Genomics Research Center, Academia Sinica; Department of Psychiatry, Cheng Hsin General Hospital, Taipei, Taiwan
6 Department of Physiology, Laboratory of Cognitive Neuroscience, National Defense Medical Center; Department of Psychiatry, Cheng Hsin General Hospital; Department of Psychiatry, Tri-Service General Hospital, Taipei, Taiwan

Date of Submission11-Jul-2021
Date of Decision24-Aug-2021
Date of Acceptance01-Sep-2021
Date of Web Publication27-Oct-2021

Correspondence Address:
Dr. Chen-Cheng Lin
Genomics Research Center, Academia Sinica, Taipei 11529
Taiwan
Dr. Yia-Ping Liu
Department of Physiology, Laboratory of Cognitive Neuroscience, National Defense Medical Center, Taipei 11490
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/cjp.cjp_63_21

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  Abstract 


Positive feeling or rewarding experience is crucial for individuals to operative their cognitive activities via an outcome evaluation of incentive reinforcement. For a long time, rewarding process or outcome evaluation is assumed greatly influenced by neuronal construct that holds individuals' impulsiveness, a capacity to inhibit unwanted behaviors provoked in a given situation. In the present study, we proposed that the outcome evaluation or rewarding experience can influence the occurrence of impulsiveness too. We hypothesized that animals would be more likely to deliver impulsive action in the place where it was previously associated with reinforcing process, in which central dopamine may play an important role. By employing five-choice serial reaction time task (5-CSRTT), we examined whether one of the five holes where rats made a correct response to get the reward would gain a higher probability to deliver premature or perseverative activities than other holes in the next trial of 5-CSRTT under baseline or longer waiting period condition. The effects of D1 receptor antagonist SCH23390 were also evaluated in the above paradigm. We demonstrated that (i) the influence on motoric impulsive response from previous rewarded experience can be described in a behavioral paradigm such as the 5-CSRTT, (ii) both prematures and perseverations at the hole associated with previous rewarding were about one-fifth of probability, however were statistically not correlated unless the interventions of inter-trial interval = 7 plus SCH23390, and (iii) the hole associated with the positive reinforcement of the 5-CSRTT appears more likely for rats to carry out an intuitive impetus under SCH23390 in a longer waiting condition. Our results may shed some insight toward the role of rewarding process in impulsive behavior.

Keywords: Dopaminergic D1 receptors, five-choice serial reaction time task, impulsivity, positive reinforcement, reward


How to cite this article:
Chen TH, Chen YJ, Huang TS, Hsiao M, Lin CC, Liu YP. Does positive feeling lead to more impulsiveness? – Implication of previous rewarded experience on location-dependent motoric impulsivity. Chin J Physiol 2021;64:218-24

How to cite this URL:
Chen TH, Chen YJ, Huang TS, Hsiao M, Lin CC, Liu YP. Does positive feeling lead to more impulsiveness? – Implication of previous rewarded experience on location-dependent motoric impulsivity. Chin J Physiol [serial online] 2021 [cited 2021 Nov 27];64:218-24. Available from: https://www.cjphysiology.org/text.asp?2021/64/5/218/329363

Tsung-Hua Chen and Yu-Jung Chen: Equally contributed to this study.





  Introduction Top


Individuals' conduct is highly associated with outcome evaluation, particularly in terms of psychological process of rewarding, which is a positive feeling for them to keep doing things. In goal-directed instrumental task, individuals are required to control their response, and they need to be equipped to prime the action, to execute the action, and most importantly, to estimate the consequence of the action.[1],[2]

Incentive value of the reward may influence the contingency between impulsive action and the reinforcing outcome.[3] Thus, for a long time, rewarding process or outcome evaluation is assumed greatly influenced by neuronal construct that holds individuals' impulsiveness; the latter is thus considered as a capacity to inhibit certain unwanted behaviors provoked in a given situation.[4] In fact, adjustment of impulsivity is one of the key factors in response control.[5] In favor of overall advantage, proper behavioral inhibition is necessary and justified. It restrains the impetus not to act intrusively, although sometimes at the expense of making additional efforts.[3]

In general, clinical data show that dysfunction of impulse control may change the sensitivity in rewarding process or lead to bias of outcome evaluation (for example, by delayed reward discounting), as seen in drug addiction/dependence and other impulsive conditions, such as gambling disorders.[6],[7],[8],[9] Specifically, a human study showed that impulsivity can be used to predict psychopathological symptoms in individuals with higher sensitivity to reward,[10] which contributes to the development of addicted behavior.[11]

In contrast to what had been mentioned above, increasing evidence indicates that outcome evaluation can influence impulsiveness too. It is noticed that the valuing process of incentive reward is involved in the regulation of response control,[12],[13] in which the misinterpretation of rewarding outcomes may lead to impulsive behavior.[14] By introducing an idea of topographical influence, O'Connor et al. went a step further to suggest that the location of reward located can be a determinant for impulsive behavior to take place. With virtual reality technology, they demonstrated that more proximal to reward, more impulsive activities occurred.[15]

The study we present here is along with the idea that impulsiveness can be affected by outcome evaluation. However, in addition to the proximity of reward as O'Connor et al. demonstrated,[15] we hypothesize that impulsiveness occurred in the place just being successfully rewarded should gain a higher probability than random distribution. This can be examined by assessing how impulsivity is distributed across all possible locations in a multiple-choice task.

To test the hypothesis, a well-designed behavioral paradigm recording impulsive action across all locations that could be chosen is required. In rats, impulsivity occurring in the five-choice serial reaction time task (5-CSRTT) is categorized as a motoric activity; it exemplifies an abrupt action initiated prior to the stage of information collection, which is accordingly less thoughtful but more intrusive.[2],[16] In the 5-CSRTT, rats have to pay attention to the array of holes in a designed apparatus to detect the discriminative visual stimulus and then to poke the correct hole to earn reward. Response occurring before the appearance of the stimulus is recorded as a premature action, which can be used to reflect animals' motoric impulsivity.[17] The 5-CSRTT provides independent and reliable indexes of rats for their attentional accuracy and inhibited response control.[18] In this task, premature refers to the response during the time waiting for the emergence of visual signal, while perseveration is an additional behavioral output after the necessary response. 5-CSRTT is therefore useful in testing the hypothesis whether previous rewarding outcome may serve as a crucial determinant for the animal to adjust its ongoing impulsivity. On the other hand, since dopamine (DA) plays an important role that links the reward outcome and behavioral activation/inhibition,[19] it is highly involved in the reward outcome-related impulsivity and the willingness of waiting.[19] Manipulation of DA D1 receptors would be employed to adjust the impulsive behavior in 5-CSRTT under conditions of baseline waiting and longer waiting.[19]

In brief, the present study demonstrated how we employed the 5-CSRTT to test the hypotheses that rewarded positive feeling could influence later on impulsiveness in a location-dependent manner, and whether there is any possible relevance to central DA. The results may shed some insight toward the understanding regarding the role of rewarding process in impulsive behavior.


  Materials and Methods Top


Animals

A total of 32 male Sprague-Dawley rats (BioLASCO, Taiwan) were used. All rats were housed in groups of three and in a temperature- and humidity-controlled holding facility with 12-h light/dark cycles (light on from 07:00 to 19:00). All animals received ad libitum water. However, food was restricted so that it could be earned during the test sessions [maximum of 100 mg × 45 mg purified rodent pellets (LabDiet, USA)] and 20 g/rat standard rodent chow (BioLASCO, Taiwan) at the end of the test. Rats were trained to learn the 5-CSRTT at an age of 12 weeks. They reached the criteria for the 5-CSRTT at an age of 16 weeks with body weight of 300–350 g. All experimental procedures were evaluated and approved by the Animal Care Committee of National Defense Medical Center (IACUC-19-093).

Five-choice serial reaction time task and behavioral manipulations

The training program was identical to that of a previously described procedure.[20],[21],[22] Each session began with the illumination of the 5-CSRTT chamber (25 cm × 31cm × 33 cm3, TSE Systems GmbH, Bad Homburg, Germany) with a house light. The rats had to nose poke the magazine in order to initiate a trial. After a fixed inter-trial interval (ITI) of 5 s, the light at the rear of one of the response apertures was briefly illuminated. A response in this aperture within a limited time from illumination of the hole (limited hold period) was recorded as a correct response and was rewarded by delivery of a food pellet to the magazine. Response in a non-illuminated hole was recorded as an incorrect response and was punished by a 5-s timeout period, during which the house light was extinguished. A session was either terminated after a maximum of 100 completed trials or 30 min, depending on which came first.

Accuracy was measured by the percentage of correct responses [correct responses/(correct responses + incorrect responses)]. Responses in any one of the apertures prior to the illumination (i.e., during the ITI) were recorded as prematures (the first response) and “perseverations during ITI (additional responses following the first response).” Perseverative responses at the hole after correct nosepoking were also recorded as “perseverations after correct response” to reflect the impetus immediately after the correct nose poke.[23] Premature/perseveration at the hole linked to successful rewarding experience in the previous trial was monitored as “previous reward-associated premature/perseveration.” In behavioral manipulations, for assessing animals' waiting capacity, the ITI was adjusted to 7 s in separated testing sessions.

Drug

SCH23390 (Sigma, USA) was dissolved in 0.9% saline (SAL, as vehicle). It was freshly prepared prior to their use, and all injections were made intraperitoneally. SCH23390 or SAL was injected 30 min before the 5-CSRTT. The dosage of SCH23390 (5 μg/kg) was chosen for highlighting the D1 effect on constraining the impulsivity,[24] which is expected to be prompted by long ITI condition.

Data and statistical analysis

A multiple-way ANOVA was conducted with DRUG (i.e. SCH23390 vs. SAL) as between-subject factor and CONDITION as within-subject factor [ITI = 5 (baseline) vs. ITI = 7]. When an interaction was found, the data were further split to obtain the simple main effect. In addition, planned comparisons were employed for a better clarification of the data, in which Student's t-test was used where appropriate. Mann–Whitney rank-sum test was applied if the Student's t-test failed in either normality test or equal variance test. Pearson method was applied for impulsivity profiles. The statistical significance of probability level was set at 0.05.


  Results Top


For percentage of accuracy, ANOVA revealed that there were no main effects of CONDITION or DRUG and no effect of CONDITION × DRUG [Figure 1].
Figure 1: Rats' attentional performance (correct response, in %) of the effects of SCH23390 under baseline (inter-trial interval = 5) and challenged condition (inter-trial interval = 7 s). Values are presented as mean ± standard error of the mean (SEM) (N = 8 for each group).

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Long ITI provoked more total prematures which could be reversed by SCH23390 (CONDITION × DRUG [F(1,14) = 9.02, P < 0.01]; main effect of CONDITION [F(1,14) = 10.55, P < 0.01]). For previous reward-associated prematures, they were elevated in long ITI condition (main effect of CONDITION [F(1,14) = 15.72, P < 0.001]). Further analysis was made for the ratio of previous reward-associated premature/total premature. SCH23390 group had higher ratio in ITI = 7 (P = 0.038, by Mann–Whitney rank-sum test) than hypothetical probability of one of the five choices (i.e. 20%) [Figure 2].
Figure 2: Effects of SCH23390 on rats' impulsive performance under baseline (inter-trial interval = 5) and challenged condition (inter-trial interval = 7 s) on total premature (a), previous reward-associated premature (b), and the ratio of previous reward-associated premature to total premature (c), compared with 20%, which is the one-fifth probability of the total count, i.e. randomized distribution across five holes). SCH23390 attenuated total (i.e. the randomized) prematures/perseverations but not the previous reward-associated prematures under a longer information-waiting period. SCH23390 rats exhibited a motoric preference to the location linked to previous reinforcement under a longer information-waiting period (inter-trial interval = 7 s). Values are presented as mean ± standard error of the mean (SEM) (N = 8 for each group). *P < 0.05, **P < 0.01, *** P < 0.001.

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For total ITI preservations, they were increased in long ITI condition which could be reversed by SCH23390 (CONDITION × DRUG [F (1,14) =9.66, P < 0.01]; main effects of CONDITION [F (1,14) =16.28, P < 0.001] and DRUG [F(1,14) = 9.04, P < 0.01]). For the previous reward-associated ITI preservations, there were main effects of CONDITION (F(1,14) = 10.73, P < 0.01) and DRUG (F(1,14) = 8.98, P < 0.01), revealing that previous reward-associated ITI preservations would be increased in long ITI condition. For the ratio of previous reward-associated ITI preservation/total ITI preservation, there were no main effects of CONDITION or DRUG and no effect of CONDITION × DRUG [Figure 3].
Figure 3: Effects of SCH23390 on rats' impulsive performance under baseline (inter-trial interval = 5) and challenged condition (inter-trial interval = 7 s) on total inter-trial interval perseverations (nose poking after the premature) (a), previous reward-associated inter-trial interval perseveration (b), and the ratio of previous reward-associated inter-trial interval perseveration to total inter-trial interval perseveration (c). SCH23390 attenuated total perseverations but not the previous reward-associated perseverations under a longer information-waiting period. Values are presented as mean ± standard error of the mean (SEM) (N = 8 for each group). *P < 0.05, **P < 0.01, *** P < 0.001.

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SCH23390 increased the count of preservations after correct nosepoking in baseline, but not long ITI condition (CONDITION × DRUG [F(1,14) = 8.11, P < 0.05]; main effect of CONDITION [F(1,14) = 7.46, P < 0.05]) [Figure 4].
Figure 4: Rats' performance of perseverations after correct nose poking of the effects of SCH23390 under baseline (inter-trial interval = 5) and challenged condition (inter-trial interval = 7 s). Values are presented as mean ± standard error of the mean (SEM) (N = 8 for each group). *P < 0.05, **P < 0.01.

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Finally, the correlations among the counts of total premature, total ITI perseverations, previous reward-associated premature, previous reward-associated preservation, and perseverations after correct nosepoking were also analyzed. Significantly positive correlations were found among total prematures and total ITI perseverations (r = 0.83, P = 0.0108), total prematures and previous reward-associated prematures (r = 0.919, P = 0.00125), total ITI perseverations and previous reward-associated prematures (r = 0.886, P = 0.00342), and total ITI perseverations and previous reward-associated perseverations (r = 0.802, P = 0.0167) in SCH23390 group in ITI = 7 [Table 1].
Table 1: The correlations among the counts of total premature, total ITI perseverations, previous reward-associated premature, previous reward-associated, and perseverations preservation after correct nosepoking (n=8)

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  Discussion Top


In the present study, we suggested that goal-directed process and stimulus–response habit, the two major factors controlling instrumental behavior, can be interactively linked,[1],[25] as the responding habit/propensity can be influenced by the reward-oriented instrumental context. We demonstrated that the psychological meanings of total premature and previous reward-associated premature are different. Total premature indicates an intrusive impulsiveness, which is without any pre-determined inclination to act out the impulsiveness. Regarding previous reward-associated premature, it inherits more goal-related impulsive nature, as it operates in the same place of action that leads to previous reward. We also found that not only impulsivity can affect the rewarding processing, but in a reversed manner, the occurrence of impulsiveness could be subjected to the outcome evaluation. We further showed that in a long waiting condition, the hole associated with the positive reinforcement of the 5-CSRTT appears more likely for rats to carry out an intuitive impetus under SCH23390, a DRD1 antagonist. As to the perseverative responding, it represents excessive activities or behavioral activation with impulsive nature in the location where the cue of reward appears.[26],[27] Specifically, the location context associated with previous positive reinforcement can be regarded as a conditional stimulus (CS, as in the study of conditioned place preference[28]) which is highly relevant to impulsivity according to the autoshaping model of drug abuse.[27],[29],[30] Note, although both prematures and perseverations at the hole associated with previous rewarding were about one-fifth of probability, they were statistically not correlated [Table 1] unless the interventions of SCH23390 at ITI=7 condition. It suggested that these two variables are independent in baseline, yet correlated to each other under a longer waiting time and when D1 is blocked, possibly referring to a greater challenge of response control.

The present study demonstrated that reward-associated behavior is not restricted in the relationship between the decision-making and goal selection as previously thought,[31] it applies to impulsivity or behavioral inhibition, too.[13] Impulsivity is a psychological term with heterogeneous natures. Impulsivity with cognitive nature is different from that with motoric one. For example, reward-associated impulsivity in delayed reinforcement task (DRT) is an action of choosing between small reward with shorter waiting time and large reward with longer waiting time, thus it is considered with more cognitive component.[2],[16] In contrast, impulsivity in 5-CSRTT is less thoughtful, more intrusive and is an excessive/compulsive activity that occurs exactly during the time of waiting, rather than any action of choosing. Both the premature and perseverative activities measured in the 5-CSRTT of the present study represented failures of behavioral inhibition of response control. Our finding that more intuitive impetus delivered in the location where it just led to reward is possibly to be clinically implicated by continuous perseveration as a symptom of frontal lobe dysfunction,[32] or a compulsive nature due to problems of corticostriatal pathway.[33]

Noted in baseline condition where the waiting time for visual stimulus (i.e. ITI) was set at 5 s, both prematures and perseverations at the hole associated with previous reward were about one-fifth of probability, indicating they may be at a similar level of failure of response control. We demonstrated that although rats' performance of visuospatial attention was goal directed, their impulsivity profile was unintentional/randomly distributed across those five holes. In other words, it is clear that goal-directed attentional function and stimulus–response habit were not linked. Since there were no statistical correlations between prematures (i.e., activities before the emergence of signal indicating the reward) and perseverations (i.e. activities immediately after the correct nosepoking, it appears unlikely due to a “liking to wanting” connection as applied in the interpretation of the development of addiction).[34]

More interestingly, following the intervention of SCH23390, behavioral manipulation of prolongation of the waiting period (i.e. by lengthening the ITI from 5 to 7 s) became associated the goal-directed process and the stimulus–response habit. Our SCH23390 data may have multiple-fold implications. First, cognitive impulsivity (which is also highly affected by DA manipulation) and motoric impulsivity (as addressed in the 5CSRTT) are overlapped to a degree. Second, the blockade of D1 receptors effectively reduced the number of premature responding in the condition of ITI = 7, in line with the evidence that the drug may reduce the motoric impulsivity in situation where the behavioral disinhibition is liable to prompt.[35] Third, SCH23390 attenuated the randomized premature/perseveration but not the habitual (or intentional) premature/perseveration, indicating the inconsistency of responding impetus and goal-directed process was possibly due to the devaluation of reward by D1 antagonism.[36] Fourth, the blockade of D1 receptors may potentiate synaptic DA to act on D2 receptors, which can possibly lead to increase D2-activated perseverative responding, as seen in the quinpirole study.[37] Finally, taken together the effects of SCH23390 that (i) to reduce the total premature and previous reward-associated premature but (ii) to increase the “ratio of previous reward-associated premature to total premature” in prolonged waiting (ITI = 7) conditions, it is possible that in long waiting challenged condition, habitual vigor/impetus is contingently reward-related rather than randomly distributed.[27] This can be supported by the strong correlation between total premature/perseveration and previous reward-associated premature/perseveration when ITI = 7.

There are certain concerns/limitations that need to be addressed. First, our interpretation of impulsivity could be confounded by reference memory error, as suggested by Sontag et al. that rats with higher error rate were difficult to separate previously baited and nonbaited locations in a hole-board paradigm.[38] Second, setting 20% as an average of impulsivity occurrence across five holes was an assumption; it needs to be comprehensively validated by analyzing the distribution of impulsivity. Third, there was a lack of dose-dependent approach of SCH23390 in our study, thus the interpretation needs to be cautious. Finally, when considering the habitual premature really links to the topographic location of rewarding context of the previous trial, rats' immediate or short-term memory could be possibly affected by SCH23390. Since both beneficial and harmful effects of SCH23390 on memory have been reported,[38],[39],[40] that is necessary to be clarified in the future.


  Conclusion Top


In summary, our results suggested that responding habit/propensity can be influenced by the reward-oriented instrumental context with a location-dependent manner. Two major factors controlling instrumental behavior, goal-directed process and stimulus-response habit, can be interactively linked.[1],[25]

Financial support and sponsorship

This research was supported by grants from the Ministry of Science and Technology (MOST 105-2410-H-016-002-MY2, 107-2410-H-350-001, 108-2623-E-350-001-D, and 108-2410-H-350-001-MY2), National Defense Medical Center (MAB102-83, MAB-107-051, MAB-108-062, and MAB-109-052), Hualien Armed Forces General Hospital (805-C107-06, 805-C108-18, HAFGH-E-109016, and HAFGH-D-110011), Cheng Hsin General Hospital and National Defense Medical Center (CH-NDMC-108-9, CH-NDMC-109-7, and CH-NDMC-110-9), and Tri-Service General Hospital (TSGH-C106-107) of Taiwan.

Conflicts of interest

There are no conflicts of interest.



 
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