Suboptimal choice by pigeons is eliminated when key-pecking behavior is replaced by treadle-pressing
Introduction
The suboptimal choice procedure has been employed in a long list of studies, with the objective of studying the determinants of choice and to model in animals some aspects of human gambling behavior. In the prototypical procedure (Stagner and Zentall, 2010), pigeons choose via a key peck between: a) an alternative (discriminative) that in 20 % of the trials presents a stimulus that predicts the delivery of a reinforcer 10 s later and that in 80 % of the trials presents another stimulus that predicts that 10 s later, no reinforcer will be delivered (overall probability of reinforcement = .20), and b) another alternative (non-discriminative) that presents either of two stimuli that equally predict that 10 s later a reinforcer will we delivered with p = .50 (overall probability of reinforcement = .50). The name of the procedure is derived from the fact that pigeons have a strong preference for the first alternative, i.e., the discriminative and suboptimal.
Even though the strong preference for the suboptimal alternative has been replicated dozens of times in pigeons (for reviews, see Zentall, 2016; McDevitt et al., 2016), its generality remains largely unexplored as key pecking is the only response that has been studied in pigeons, and few experiments have studied other species. Performing research with other responses and species would undoubtedly help to elucidate the mechanisms that promote suboptimal choice; an example of the usefulness of this approach is (though not consensual) the postulation of the incentive salience of the discriminative stimuli (Chow et al., 2017) as source of the difference between pigeons’ suboptimality (Zentall, 2014) and rats’ optimality (Trujano and Orduña, 2015). Incentive salience is a property of some conditioned stimuli (CS) which, due to their contingent pairing with an unconditioned stimulus (US), acquire the ability to attract behavior towards them, to function as secondary reinforcers, and to arouse complex emotional and motivational states related to the receipt of the US (Robinson et al., 2018). Incentive salience is not an absolute property of a CS, but depends, among other things, on its sensory properties (Singer et al., 2016; Meyer et al., 2014), the species used (Powell et al., 1975), and more generally, on the biological relatedness between the CS and the US for that particular species (Timberlake and Grant, 1975; Zentall et al., 2019). Interestingly, it has been reported that even when different organisms from the same species are exposed in a contingent way to the same pair of CS-US (e.g., lever-food), there are striking individual differences in the incentive salience attributed to the conditioned stimulus (Meyer et al., 2012). Incentive salience is a solid construct, with all its causes (Killeen, 2001): final (Nesse and Berridge, 1997; Newlin, 2002), efficient (Tomie et al., 2014), material (Kuhn et al., 2018) and formal (Anselme, 2015; McClure et al., 2003; Zhang et al., 2009), as well as some of its implications in the promotion of maladaptive behavior (Meyer et al., 2018) extensively investigated.
When applied to the issue of between-species differences in suboptimal choice, the incentive-salience hypothesis basically proposes that such differences are a byproduct of differences in the incentive salience of the discriminative stimuli employed with each species: while for pigeons the stimuli are usually illuminated keys which have high incentive salience for them and evoke sign-tracking responses that persist even when they cancel the presentation of food (Williams and Williams, 1969), the stimuli employed in the first studies with rats were lights (Trujano et al., 2016; Trujano and Orduña, 2015) or sounds (Ojeda et al., 2018), which do not have incentive salience for this species as they provoke goal-tracking behavior (Beckmann and Chow, 2015). The hypothesis that relates incentive salience of the stimuli with suboptimal preferences has been evaluated in rats, without conclusive results; although the first study reported that using levers as discriminative stimuli -which have been shown to be attributed with higher incentive salience than lights or tones (Beckmann and Chow, 2015)- promoted suboptimal choice (Chow et al., 2017), this result has not been replicated (Martinez et al., 2017; López et al., 2018; Orduña and Alba, 2019; Alba et al., 2018).
If we accept the idea that illuminated keys for pigeons and levers for rats have an equivalent level of incentive salience for the respective species, the results revised so far suggest that the incentive salience of stimuli is not the variable underlying their differential performance in the “suboptimal choice” procedure. It is possible, however, that although rats attribute more incentive salience to levers than to lights or tones (Beckmann and Chow, 2015), the level of incentive salience is lower than the level that pigeons attribute to illuminated keys, and does not reach the threshold for generating suboptimal choice. If pigeons preferences in the suboptimal choice procedure are actually influenced by the incentive salience of the stimuli, a decrement in pigeons’ suboptimal behavior should be expected if the discriminative stimuli are separated from the response manipulandum (Tomie, 1996), and if the response manipulandum does not elicit the same consummatory behavior than the reinforcer. In support of this argument, different sources of evidence suggest that several instances of pigeons’ maladaptive key-pecking behavior are derived from the strong influence that Pavlovian contingencies have on pecking behavior; this influence is maximal in conditions in which the discriminative stimuli are presented on the response key (LoLordo, 1971; Boakes et al., 1975), smaller when the stimuli are separated from the response key (Westbrook, 1973), and is absent in conditions in which key pecking is replaced by foot-pressing a treadle (Westbrook, 1973; Green and Holt, 2003; LoLordo et al., 1974). It has been reported, for example, that pigeons are less efficient in differential reinforcement of low rates schedules when the operant response is key pecking than when it is treadle pressing (Hemmes, 1975). In a temporal discounting task, pigeons show a higher degree of discounting when the choice response is key pecking than when it is treadle pressing (Holt et al., 2013). The differences between these operant responses have also been noted in experiments exploring behavioral contrast: When pigeons are trained in multiple variable interval (VI)-VI schedules, and one of the schedules is changed to extinction, pigeons increase their response rate in the unchanged component when the operant response is key pecking, but show no changes when the operant response is treadle pressing (Hemmes, 1973).
The particularities of key pecking as an operant response have also been noted in the context of species differences in the sensitivity to the addition of free reinforcers to one of the components of a multiple schedule VI 2 min VI 2 min (Boakes et al., 1975); while pigeons’ key pecking increased during the component with free reinforcers added, rats’ lever pressing decreased in this component. In a similar experiment, the effect of adding free reinforcers was observed for pigeons’ key pecking, but not for pigeons treadle pressing (Green and Holt, 2003; LoLordo, 1971; LoLordo et al., 1974).
All this evidence is compatible with the idea that key pecking is strongly influenced by the Pavlovian contingency between the stimuli displayed on the keys and the reinforcer, and less sensitive to the instrumental contingencies between key pecking and reinforcers than other responses like treadle pressing. Coherently with this line of arguments, it has been suggested that “treadle pressing in pigeons is more comparable to the operant behavior shown by other species than is key pecking” (Hemmes, 1975; p 356).
It is possible, then, that the mechanism by which the treadle-pressing response diminished maladaptive behavior in the studies described above was a decrement in the incentive salience, which was favored by both the separation between the discriminative stimuli and the response manipulandum, and by the dissimilarity in topography between the operant response and the consummatory responses originally elicited by the US (Zentall et al., 2019). In this context, we hypothesized that the suboptimal behavior of pigeons could be diminished by presenting ambient lights as discriminative stimuli, instead of the usual illuminated keys, and by replacing key pecking by treadle pressing as the choice response.
Section snippets
Subjects
Eleven naive, domestic pigeons (Columba livia) of undetermined sex and between 1 and 2 years old served as subjects. Their weight when they were not food-restricted was 402 ± 77.3 g (Mean ± SD). At the beginning of the experiment, subjects were food deprived until they reached 80 % of their ad libitum weight; throughout the experiment subjects received food after the experimental sessions when needed to maintain the intended weight. All experimental protocols followed the Official Mexican
Treadle-pressing condition
Fig. 2 shows, for each subject, the proportion of choice for the discriminative alternative during each of the sessions of the “suboptimal choice” training and its reversal phase in the condition in which the operant response was treadle pressing; once the stability criteria were met, the last five sessions of each phase were used for statistical purposes. The group’s proportion of choice for the discriminative alternative during the last five sessions of training was .23 ± 0.10 (Mean ± SEM),
Discussion
In the present study, we made a twofold modification of the classical procedure employed to study suboptimal choice by pigeons. On the one hand, we manipulated the operant response by which pigeons chose between a discriminative alternative associated with a lower probability of reinforcement and a non-discriminative alternative associated with a higher probability of reinforcement. On the other hand, we presented ambient stimuli, separated from the response manipulandum, instead of the
Author contributions
V.O. conceptualized the experiments, developed the experimental design and wrote the manuscript. R.G and J.F. contributed to the development of the experimental design, performed the experiment, analyzed the data and reviewed the manuscript.
Acknowledgements
This research was supported by grants 281548 from CONACYT and IN306818 from PAPIIT-DGAPA. We thank Fernando Salinas for technical assistance, Enrique Rivera for assistance in data collection and experimental design of pilot experiments, and Rodrigo Alba for help in animal care and data analysis.
References (60)
- et al.
Rats’ preferences in the suboptimal choice procedure: evaluating the impact of reinforcement probability and conditioned inhibitors
Behav. Processes
(2018) Incentive salience attribution under reward uncertainty: a Pavlovian model
Behav. Processes
(2015)- et al.
Suboptimal choice in rats: incentive salience attribution promotes maladaptive decision-making
Behav. Brain Res.
(2017) Pigeons’ performance under differential reinforcement of low rate schedules depends upon the operant
Learn. Motiv.
(1975)- et al.
Response factors in delay discounting: evidence for Pavlovian influences on delay discounting in pigeons
Behav. Processes
(2013) - et al.
The effects upon food-reinforced pecking and treadle-pressing of auditory and visual signals for response-independent food
Learn. Motiv.
(1974) - 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.
A computational substrate for incentive salience
Trends Neurosci.
(2003) - et al.
Paradoxical choice in rats: subjective valuation and mechanism of choice
Behav. Processes
(2018)