Research reportEffect of orbitofrontal cortex lesions on temporal discounting in rats
Highlights
► Temporal discounting of the rat was studied using a novel inter-temporal choice task. ► Rat's choices were better explained by hyperbolic than exponential discount functions. ► Two-parameter discount functions were superior to single-parameter discount functions. ► Orbitofrontal cortex lesions did not alter rat's inter-temporal choice behavior.
Introduction
Humans and other animal species preferentially choose an immediate reward over a similar, but more delayed reward, suggesting that the subjective value of a reward is discounted as a function of its delay. Temporal discounting in humans has initially been proposed to be exponential, such that the subjective value is discounted at the same rate during the entire delay [33]. However, subsequent empirical studies have repeatedly shown that temporal discounting in humans is better described by a hyperbolic discount function than by an exponential function [7], [27]. Similar results have been reported for rats [20], [21] and pigeons [21], [29], suggesting that hyperbolic temporal discounting might be a universal form of value discounting across different animal species. However, previous studies in rats and pigeons have employed the adjusting delay procedure [18] or block-wise variation of delay durations (e.g., [11], [16]). Such procedures often lead to choices that are non-stationary or serially correlated across trials, which can potentially lead to biases in estimating temporal discount functions [5]. By contrast, recent behavioral studies in monkeys have employed an intertemporal choice task with symbolic cues and randomized reward delays, and have shown that their choice behavior is in general more consistent with hyperbolic than exponential discounting of subjective values [3], [9], [12].
The first goal of this study was to estimate the precise form of temporal discount function in rodents, using a novel intertemporal choice task in which the sequence of delay durations was randomized across trials. The results showed that a hyperbolic discount function accounted for the rat's temporal discount function better than an exponential function. The second goal was to examine the role of orbitofrontal cortex (OFC) in temporal discounting during intertemporal choice of rats. OFC lesions are known to induce impulsive choice behavior in humans [1], [2]. Neural activity in the monkey OFC is also correlated with temporally discounted values [30]. However, previous lesion studies in rats have yielded conflicting results on this matter. Following OFC lesions, the rate of temporal discounting increased [11], [24], [32], decreased [37], did not change [6], [17], or varied depending on the extent of lesions [16] and the presence or absence of a distinct cue bridging the delay between choice and reward delivery [38]. In the present study, we tested the effect of OFC lesions on the rat's temporal discount functions that were estimated more accurately than in the previous studies. In particular, to distinguish the OFC role in learning response–outcome contingency [36] from its contribution to temporal discounting, we extensively trained rats before the lesions. We found that OFC lesions did not make a significant change in temporal discounting of rats.
Section snippets
Subjects
Seven young male Sprague-Dawley rats (approximately 9–11 weeks old, 390–400 g) were used. The animals were individually housed in a colony room and initially allowed free access to food and water with extensive handling for 1 week. Their body weight was gradually reduced to 80–85% of their free-feeding weight by water deprivation and maintained at this level throughout the study. Experiments were performed in the dark phase of a 12-h light/dark cycle. The experimental protocol was approved by
Extent of lesions
Fig. 2 shows schematic representations of the largest (light gray), medium (dark gray), and the smallest (black) OFC lesions (n = 7 animals). As shown, quinolinic acid injections consistently produced extensive damages to the medial, lateral, ventral and dorsolateral OFC [26].
Choice behavior
The animals performed 2263 ± 711 and 2343 ± 440 trials in S0 and S3 sessions, respectively, before the OFC lesions, and 1371 ± 451 and 1474 ± 206 trials in S0 and S3 sessions, respectively, after the OFC lesions (mean ± SD). When the
Discussion
The first goal of the present study was to determine the precise form of temporal discounting in rodents while avoiding methodological complications associated with the adjusting delay procedure. To accomplish this, all reward delays were explicitly signaled to the animals by the arm locations (rather than requiring the animals to estimate them through experience) and their sequence was randomized across trials in our task. Hence, our task was free from the problem of serial correlation or
Acknowledgments
This work was supported by the Research Center Program of Institute for Basic Science, the National Research Foundation grant (2011-0015618) and the Original Technology Research Program for Brain Science (2011-0019209) funded by the Ministry of Education, Science and Technology, Korea (M.W.J.) as well as a grant (R01 DA029330) from the National Institute of Health, USA (D.L.).
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GABA<inf>B</inf> receptors in prelimbic cortex and basolateral amygdala differentially influence intertemporal decision making and decline with age
2022, NeuropharmacologyCitation Excerpt :In fact, higher intertemporal discounting rates associate with poor healthcare choices and outcomes in older adults (65+ years of age; Axon et al., 2009; Bradford, 2010; James et al., 2012). Intertemporal choice is mediated by a network of cortico-striatal-amygdalar circuitry (Berlin et al., 2004; Feja et al., 2014; Gourley et al., 2010; Hosking et al., 2014; Jo et al., 2013; Mar et al., 2011; Massar et al., 2015; Mobini et al., 2002; Walton et al., 2009; Winstanley et al., 2004) that includes the medial prefrontal cortex (mPFC; rodent homologue of the human DLPFC; Brown and Bowman, 2002; Uylings et al., 2003; Kesner and Churchwell, 2011; Bizon et al., 2012) and basolateral amygdala (Churchwell et al., 2009; Winstanley et al., 2004), in addition to several neuromodulatory systems (Anderberg et al., 2016; Aurelian et al., 2016; Joutsa et al., 2015; Smith et al., 2016; Winstanley et al., 2006). Functions supported by the mPFC (and particularly the prelimbic subregion of mPFC: PrL) such as working memory, behavioral flexibility, and appetitive behaviors (Floresco et al., 2008b; Ishikawa et al., 2008; Sloan et al., 2006; Zeeb et al., 2015) are foundational to time-based decision making (Hernandez et al., 2017; Hinson et al., 2003; Huckans et al., 2011).
A framework for understanding and advancing intertemporal choice research using rodent models
2017, Neurobiology of Learning and MemoryCitation Excerpt :Although humans with OFC lesions consistently exhibit impulsive choices (Bechara, Tranel, & Damasio, 2000; Berlin et al., 2004; Sellitto, Ciaramelli, & di Pellegrino, 2010), there are discrepancies between reported effects of manipulating the rodent OFC. Following lesion or inactivation of the whole OFC, rodents’ discounting increased (Mobini et al., 2002; Rudebeck, Walton, Smyth, Bannerman, & Rushworth, 2006), decreased (Kheramin et al., 2002; Mar, Walker, Theobald, Eagle, & Robbins, 2011; Winstanley, 2004), or did not change (Abela & Chudasama, 2013; Churchwell, Morris, Heurtelou, & Kesner, 2009; Jo, Kim, Lee, & Jung, 2013; Mariano et al., 2009; Moschak & Mitchell, 2014). The reasons for the inconsistencies are not fully known, but one possibility is that the OFC was differentially engaged based on the experimental design.
Individual differences in impulsive action and dopamine transporter function in rat orbitofrontal cortex
2016, NeuroscienceCitation Excerpt :In addition to impulsive action, OFC is implicated in impulsive choice, as increases in impulsivity are observed following excitotoxic lesions of this region (Kheramin et al., 2002, 2004; Mobini et al., 2002; Rudebeck et al., 2006). Other studies have reported either a decrease or no change in impulsive choice following lesions to OFC (Winstanley et al., 2004; Mariano et al., 2009; Mar et al., 2011; Abela and Chudasama, 2013; Jo et al., 2013). These discrepancies may result from differential destruction of subregions of OFC, as lesions to medial OFC increase sensitivity to delayed reinforcement, whereas lesions to lateral OFC decrease impulsive choice (Mar et al., 2011).
Dissociable roles of dopamine and serotonin transporter function in a rat model of negative urgency
2015, Behavioural Brain ResearchCitation Excerpt :Evidence also shows that OFC is involved in impulsive behavior, although some inconsistencies exist in the literature. For example, several studies have reported an increase in impulsive choice following lesions to OFC [46–49]; however, other studies have observed either a decrease in impulsive choice [50,51] or no change in impulsive choice following temporary inactivation via GABA agonists or following excitotoxic lesions [52–56]. Despite these discrepancies regarding impulsive choice, damage to OFC increases impulsive action [57,58].
Partial inactivation of nucleus accumbens core decreases delay discounting in rats without affecting sensitivity to delay or magnitude
2014, Behavioural Brain ResearchCitation Excerpt :Conversely, the role of the OFC is less clear. Some studies have found that lesions increase delay discounting [37,25,26,46], one has found that lesions decrease discounting [50], and some have found no effect [32,18,1,23]. These discrepant findings have been suggested to be the result of procedural differences [52] and/or the regional specificity of the lesions [31].