The incentive salience of the stimuli biases rats’ preferences in the “suboptimal choice” procedure
Introduction
In recent years, the suboptimal choice procedure has been extensively employed for studying the mechanisms of choice in humans (Molet et al., 2012), pigeons (Stagner and Zentall, 2010), rats (Trujano and Orduna, 2015) and other species (Vasconcelos et al., 2015), probably because of its relationship with some instances of maladaptive behavior in humans, like pathological gambling (Molet et al., 2012). In the suboptimal choice procedure, two alternatives are presented: discriminative, and non-discriminative. When the first is chosen, two different stimuli may be presented, one that signals with certainty that a reinforcer will be delivered or another that signals -also with certainty- that no reinforcer will be available. When the second alternative is chosen, either of two stimuli may be presented, both associated with the same probability of reinforcement, which is usually smaller than 1.0 -making the reinforcer uncertain- but more likely than that of the discriminative alternative, which makes it the optimal alternative. The procedure was named after pigeons showed a strong preference for the discriminative alternative despite it being associated with a lower overall probability of reinforcement (for reviews, see Zentall, 2014; McDevitt et al., 2016).
One of the unresolved issues regarding this procedure is the notable difference that has been found when comparing the performance of pigeons and rats: as stated above, in at least dozens of experiments pigeons have shown a strong and consistent preference for the discriminative alternative (Kendall, 1974; Smith and Zentall, 2016; Stagner and Zentall, 2010). In contrast, accumulating evidence shows that rats prefer the optimal alternative, even though they readily discriminate the different stimuli associated with it (Alba et al., 2018; López et al., 2018; Martinez et al., 2017; Ojeda et al., 2018; Trujano and Orduna, 2015; Trujano et al., 2016). Although different possibilities have been suggested to account for this species difference (Cunningham and Shahan, 2018, 2019; Chow et al., 2017; Trujano et al., 2016; Zentall et al., 2019), currently there is no agreement on its cause.
One of the recent hypotheses regarding this difference lies on the concept of incentive salience (Chow et al., 2017). This hypothesis is based on the fact that for pigeons, the discriminative stimuli employed in the suboptimal choice procedure are presented on keys, and it has been shown that illuminated keys evoke sign-tracking behavior in pigeons (Brown and Jenkins, 1968), which has been taken as evidence that pigeons attribute incentive salience to them. In contrast, the first experiments on suboptimal choice with rats presented lights as stimuli, which evoke goal-tracking behavior in rats (Beckmann and Chow, 2015; Boakes, 1977), suggesting that lights do not have incentive salience for them.
In this context, Chow et al. (2017) evaluated rats in a suboptimal choice procedure in which the discriminative stimuli were levers for one of the groups, and lights for a comparison group; the result was that the “levers” group showed suboptimal behavior while the “lights” group showed optimal behavior. Unfortunately, because in this study the negative outcome of the discriminative alternative was not associated with a lever, but with a blackout, it was possible that the suboptimality found by Chow et al., was due to the absence of a conditioned inhibitor, a stimulus that has been shown to impact rats’ behavior in this procedure (Trujano et al., 2016). To analyze this possibility, Martinez et al. (2017) performed an experiment in which one lever was associated with the positive outcome of the discriminative alternative and another lever with the negative one. Two additional levers were associated with the non-discriminative alternative. Under these circumstances, rats strongly preferred the non-discriminative (optimal) alternative, even though the discriminative stimuli had incentive salience.
A stronger test of the hypothesis that relates suboptimal choice with attribution of incentive salience was performed by Lopez et al. (2018); in this study subjects were classified by their capacity of attribution of incentive salience using the Pavlovian Conditioned Approach procedure, under the hypothesis that subjects with high capacity of attribution of incentive salience would show a higher level of suboptimal behavior than subjects with less capacity. However, the results indicated a high preference for the optimal alternative in both groups, suggesting either that incentive salience does not play a role in the suboptimal choice procedure, or that the influence of incentive salience was cancelled because it was shared by both alternatives. Other studies have also failed to replicate the result by Chow et al. (2017), despite the use of levers as discriminative stimuli (Alba et al., 2018; Orduña and Alba, 2019). In marked contrast to these results, in a related research area it has been shown that the incentive salience of the stimuli has a strong effect on preference. Beckmann and Chow (2015) associated in different trials the presentation of a lever or a tone with pellet delivery; after this phase, subjects were presented with a choice between these stimuli and showed a strong preference for the lever (95 % preference). This preference remained (75 % preference) even when the probability of pellet delivery in presence of the lever diminished to 0.50.
It is possible that the difference between Beckman and Chow's (2015) study and those that have reported no relationship between suboptimal choice and the incentive salience of the stimuli (Alba et al., 2018; Orduña and Alba, 2019; Martinez et al., 2017; López et al., 2018) is due to the fact that in the former study the alternatives differed in the incentive salience of their associated stimuli, while in the second group of studies the incentive salience was the same in both alternatives.
In the present study, we manipulated the incentive salience of the discriminative and the non-discriminative alternatives by employing levers in one of them, and lights in the other, in order to evaluate its impact on suboptimal choice (experiment 1). In addition, this manipulation was replicated employing samples of subjects with high and low capacity of attribution of incentive salience (experiment 2), under the hypothesis that the influence of the incentive salience would be higher in the former.
Section snippets
Subjects
Subjects were eight naïve male Wistar rats approximately 180 days old, obtained from the vivarium of the Institute of Cell Physiology, UNAM. Rats were housed in groups of four and placed on a food restriction schedule to maintain them at approximately 85 % of their free-feeding weight. The experiment followed the official Mexican norm NOM-062-ZOO-1999 ‘Technical Specification for Production, Use and Care of Laboratory Animals’.
Apparatus
Four modified operant conditioning chambers (MED Associates, Inc.,
Subjects
We employed 13 male Wistar rats, approximately 180 days old. Subjects had been previously classified according to their capacity of attribution of incentive salience (Lopez et al., (2018) and had experience in the suboptimal choice procedure (for a detailed description of categorization according to their PCA index, and of the experience of the subjects, see Lopez et al. (2018)). Six out of these subjects met the requirements (Meyer Lovic et al., 2012) for being classified as sign-trackers
General discussion
The suboptimal choice procedure has been proposed as an animal model of some aspects of human gambling behavior (Zentall and Stagner, 2010; Zentall, 2016b) and seems ideally suited for providing information about the relevance that the signals that predict a reinforcer, or its absence, have on preference (for a review, see Zentall, 2016a). Supporting the face validity of the procedure, both pigeons and humans are more influenced by the stimuli that predict wins than for those that predict
Author contributions
V.O. conceptualized the experiments, developed the experimental design and wrote the manuscript. R.A. conceptualized the experiments, performed them, analyzed the data and reviewed the manuscript
Acknowledgements
This research was supported by grants 281548 from CONACYT and IN306818 from PAPIIT-DGAPA. Rodrigo Alba was supported by a grant from CONACYT (450692) during his Ph.D. studies. We thank Fernando Salinas for technical assistance, Daniel Maldonado for assistance in data collection and Fernanda Barriga for useful comments on a previous version.
References (38)
- et al.
Rats’ preferences in the suboptimal choice procedure: evaluating the impact of reinforcement probability and conditioned inhibitors
Behav. Processes
(2018) - et al.
Suboptimal choice in rats: incentive salience attribution promotes maladaptive decision-making
Behav. Brain Res.
(2017) - et al.
Personality, addiction, dopamine: insights from Parkinson’s disease
Neuron
(2009) - et al.
Individual differences in incentive salience attribution are not related to suboptimal choice in rats
Behav. Brain Res.
(2018) - et al.
Incentive salience attribution is not the sole determinant of suboptimal choice in rats: conditioned inhibition matters
Behav. Processes
(2017) - et al.
Paradoxical choice in rats: subjective valuation and mechanism of choice
Behav. Processes
(2018) - et al.
Rats’ optimal choice behavior in a gambling-like task
Behav. Processes
(2019) - et al.
Optimal behavior by rats in a choice task is associated to a persistent conditioned inhibition effect
Behav. Processes
(2016) - et al.
Rats are optimal in a choice task in which pigeons are not
Behav. Processes
(2015) - et al.
Ultimate explanations and suboptimal choice
Behav. Processes
(2018)
Suboptimal choice by pigeons: an analog of human gambling behavior
Behav. Processes
Differences in rats and pigeons suboptimal choice may depend on where those stimuli are in their behavior system
Behav. Processes
Skewed by Cues? The Motivational Role of Audiovisual Stimuli in Modelling Substance Use and Gambling Disorders, Behavioral Neuroscience of Motivation
Dopamine D3 receptors modulate the ability of win-paired cues to increase risky choice in a rat gambling task
J. Neurosci.
Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence
Learn. Mem.
Performance on learning to associate a stimulus with positive reinforcement
Auto-shaping of the pigeon’s key-peck
J. Exp. Anal. Behav.
Suboptimal choice, reward-predictive signals, and temporal information
J. Exp. Psychol. Anim. Learn. Cogn.
Rats engage in suboptimal choice when the delay to food is sufficiently long
J. Exp. Psychol. Anim. Learn. Cogn.
Cited by (4)
An animal model of human gambling behavior
2023, Current Research in Behavioral SciencesThe essential value of the alternatives of the suboptimal choice procedure is different for pigeons and rats
2020, Behavioural ProcessesCitation Excerpt :This would suggest that the difference between the values of the alternatives is higher for pigeons than for rats, so changing the usually reported preference of pigeons (i.e. suboptimal) would need the intervention of a more powerful independent variable than changing the usually reported preference of rats (i.e. optimal). This is consistent with the lack of studies showing optimal choice in pigeons (but see González-Torres et al., 2020) and the variability that exists in the results of studies with rats, that include some findings of suboptimal choice in this species (Chow et al., 2017; Cunningham and Shahan, 2019; Orduña and Alba, 2020). The study of suboptimal choice may benefit from the use of the Bayesian approach, as it provides the possibility of comparing the distributions of probable outcomes and not only the different means.
Suboptimal Choice: A Review and Quantification of the Signal for Good News (SiGN) Model
2023, Psychological ReviewRats maintain optimal choice when facing long terminal links in a “suboptimal choice” procedure.
2021, Journal of Experimental Psychology: Animal Learning and Cognition