Reduced decision bias and more rational decision making following cortex damage

Reduced decision bias and more rational decision making following ventromedial prefrontal cortex damage. Sanjay Manohar et al. Cortex, February 11 2021. https://doi.org/10.1016/j.cortex.2021.01.015

Summary: Human decisions are susceptible to biases, but establishing causal roles of brain areas has proved to be difficult. Here we studied decision biases in 17 people with unilateral medial prefrontal cortex damage and a rare patient with bilateral ventromedial prefrontal cortex (vmPFC) lesions. Participants learned to choose which of two options was most likely to win, and then bet money on the outcome. Thus, good performance required not only selecting the best option, but also the amount to bet. Healthy people were biased by their previous bet, as well as by the unchosen option’s value. Unilateral medial prefrontal lesions reduced these biases, leading to more rational decisions. Bilateral vmPFC lesions resulted in more strategic betting, again with less bias from the previous trial, paradoxically improving performance overall. Together, the results suggest that vmPFC normally imposes contextual biases, which in healthy people may actually be suboptimal in some situations.

Discussion

In this study we used a novel reversal learning task in which participants made post-decision wagers on their choices, thereby providing a measure of their confidence in winning, and also rated their surprise at outcomes (Fig.1). Analysis was performed on both performance data as well as with a computational model of value learning. In healthy volunteers, bets tracked the expected chance of winning (Fig.4A), but also showed strong biases: People’s bets tended to be similar to their bets on the previous trial, and were higher when the unchosen option was less likely to win. Patients with unilateral mPFC lesions bet more overall (Fig.3B), but showed weaker biases from the previous trial and from the unchosen option. The bilateral patient MJ also showed a weaker bias from the previous trial (Fig.4B), but crucially had a stronger effect of the chosen option’s probability of winning (Fig.4A). This meant that he won more than any other healthy volunteer or unilateral patient on this task (Fig.2A), despite no difference in learning which option was better. Thus, his performance can be seen as exhibiting a more rational betting strategy than in healthy people.

A large body of evidence has revealed that many aspects of human decision making are seemingly irrational, driven by biases that appear to lead to suboptimal outcomes (Tversky and Kahneman, 1974; De Martino et al., 2006; Talluri et al., 2018; Urai et al., 2019). Evidence that some of these biases are driven by normal cognitive operations underpinned by specific brain processes (De Martino et al., 2006; Wimmer and Shohamy, 2012) raises the possibility that damage to the brain might paradoxically reduce such biases (Akrami et al., 2018; Kapur, 1996) and perhaps lead to more rational behaviour. However, to date only limited causal evidence for such a possibility exists in humans (Greene, 2007; Knoch et al., 2006; Koenigs et al., 2007).

The findings presented here show that it is indeed possible for more rational decision making to emerge – at least on a value based reversal learning task – after bilateral vmPFC lesions. This is not to say that all decisions and behaviours become more rational after such brain damage. Clearly, although he managed to continue to work in a demanding job, patient MJ showed evidence of dysfunction in social cognition and some aspects of decision making and judgment in everyday life, just as previous reported cases (Eslinger and Damasio, 1985; Bechara et al., 2000; Berlin et al., 2004; Shamay-Tsoory et al., 2005).

There is some previous circumstantial evidence that mPFC lesions may reduce decision biases. For example, patients with mPFC damage show smaller biases in probabilistic estimation (O’Callaghan et al., 2018), reduced affective contributions to reasoning (Shamay-Tsoory et al., 2005), and may indeed make more utilitarian moral judgements, suggesting more rational valuation with less affective bias (Ciaramelli et al., 2007; Koenigs et al., 2007; Krajbich et al., 2009). These effects might be underpinned by a more general increase in rationality after damage to this region. One possible explanation for this is that individuals with vmPFC lesions might be free of affective biases that normally contribute to such decision making but this remains to be established.

In line with this, Shiv et al. (2005) asked patients with a variety of lesions (amygdala, orbitofrontal and insula) to opt in or out of gambles with positive expected value. Controls tended to opt out especially after a loss, whereas the patients continued to bet, thus winning more. This can be compared to our win-stay analysis (Fig.3F), where MJ bet more than controls on win-stay choices, but did not bet less on lose-switch choices. Further evidence that biases can depend on specific brain areas comes from patients with insula damage, who may lose the normal tendency towards the gamblers’ fallacy (Clark et al., 2014). With this bias, participants tend to re-choose an option that previously lost (because the history of wins should balance out on average). Transcranial stimulation to lateral prefrontal cortex increases this bias (Xue et al., 2012). In our study, there is a possible analogy with the unchosen option effect (Fig.4C), where people bet less when the alternative was valuable (perhaps also because the two options should balance out on average). Unilateral ventromedial patients lost this bias. However, in our task, lesions did not affect the option decisions themselves.

Biases from previous trials may rely on information retained in working memory. Thus an important null result is that the bilateral patient was unimpaired in working memory accuracy (Table S2). He had considerable difficulty remembering verbal lists (Table 1). This memory deficit might have contributed to his lack of trial history biases. However, against this possibility, performance was normal on a specific working memory task, suggesting that the previous bet effect was not simply memory-related. Furthermore, his normal learning and decision-making indicate he was integrating and retaining the specific value information involved in the biases, making memory deficits less likely to contribute. One interpretation of the loss of bias could be that medial frontal areas are required for normal integration of the biasing or interfering information into the current decision. An alternative interpretation is that normal biases are driven by suboptimal heuristics, and that medial frontal lesions abolish these heuristics.

[Table 1. Summary of standardised neuropsychological scores for patient MJ. Impairments were seen in the verbal learning task for short delay recall and yes-no recognition. WAIS: Wechsler adult intelligence scale; WMS: Wechsler memory scale; WM: working memory; CVLT: California verbal learning test; DKEFS: Delis-Kaplan executive function system; GNT: Warrington graded naming test. Red indicates scores in the “extremely low” range (<2nd centile), and pink indicates scores in the borderline range (<10th centile).]

Patients with vmPFC/OFC lesions have previously been shown to bet more under uncertainty (Clark et al., 2008), being generally less risk averse (Bechara et al., 2000; Levens et al., 2014), and our results directly support this finding. However, bets reflect a combination of general risk seeking, confidence, biases and strategic factors. In our study, increased betting alone was insufficient to explain the bilateral patient’s advantage in this task. Instead, reduced biases may have permitted strategic betting, such as the hot hand effect or loss chasing. Interestingly, a previous study had identified that dorsomedial prefrontal lesions can increase the bias caused by eye movements during decisions (Vaidya and Fellows, 2015), but to our knowledge, no human studies have shown reduced biases after lesions in the way demonstrated here.

Information about unchosen options and recent actions may be disrupted by medial or orbitofrontal lesions (Buckley et al., 2009; Levens et al., 2014), which might thus account for the reduced biases in unilateral patients. The effect parallels a recent rodent study where parietal inactivation also paradoxically improved performance, by reducing the active bias from previous trials (Akrami et al., 2018). However, it is unclear why bilateral lesions did not attenuate this bias in MJ. Our finding of larger surprise differences between winning and losing may also match previous reports of increased emotional responses to stochastic outcomes after vmPFC lesions (Levens et al., 2014) and could parallel increases in reward sensitivity observed in these patients (Manohar and Husain, 2016).

Intriguingly, we found no consistent effects on option-selection in this task. Previous studies of classical reversal learning in patients with vmPFC lesions have shown varied effects. Patients tend to perseverate, maladaptively repeating their previous choices even after reward contingencies reverse (Fellows and Farah, 2003; Rolls et al., 1994), but other studies have found only a marginal effect (Daum et al., 1991), and yet others showed normal performance after unilateral lesions, but impaired reversal after bilateral lesions (Hornak et al., 2004). This is consistent with detailed studies in animals suggesting that impairments after OFC lesions may be mild, with medial lesions only impairing performance when discrimination is harder (Izquierdo et al., 2017; Rudebeck and Murray, 2011), and impairments potentially improved by further lesions (Stalnaker et al., 2007). Yet other work has demonstrated that vmPFC lesions produce unstable choices while preserving subjective valuation of single objects (Henri-Bhargava et al., 2012). However, we did not find any deficits in value-based selection of options in our task. This could be because the paradigm used here crucially tests the use of learned values, rather than subjective valuation or rule-following.

In non-human primate studies, brain areas encoding the values of options also encode decision confidence, such as OFC (Kepecs et al., 2008). In humans, fMRI activation increases with decision confidence in vmPFC (De Martino et al., 2013; Lebreton et al., 2015; Rolls et al., 2010; Yokoyama et al., 2010). Although some studies have demonstrated inaccurate confidence judgements after prefrontal lesions (Fleming et al., 2014), others find no deficits even with bilateral lesions (Lemaitre et al., 2018). Remarkably, disrupting anterior PFC with TMS can actually improve metacognitive confidence judgements (Shekhar and Rahnev, 2018). Thus, if medial PFC encodes variables that might bias valuation, lesions to this area should paradoxically improve performance in some situations, as observed here.

Of course, human lesion studies are inherently limited by the possibility of damage not visible on the MRI scans. Although all patients reported here had brain haemorrhages affecting the mPFC, with very little damage outside this region, the bilateral patient had suffered a traumatic injury, followed by haemorrhage. It is possible that this resulted in a different pattern of microscopic damage: although traumatic injuries may appear focal, often the functional damage can be quite widespread. This limits the conclusions that can be drawn about the causal role of medial frontal cortex specifically. However we suggest that the most likely explanation is the bilateral nature of his lesions: reward value is usually considered to be represented bilaterally in OFC (Hampton and O’Doherty, 2007; Rolls, 2015), suggesting that unilateral lesions are less likely to show manifest impairments. One difficulty with interpreting lesion studies is whether the changes reflect direct lesion effects, or compensatory strategies. The chronic nature of his lesion may be a key difference between MJ and other studies demonstrating deficits in reversal learning after vmPFC lesions (Fellows and Farah, 2003; Rolls et al., 1994). This may have allowed recovery and adaptation, leading to his strategic betting pattern. In this case, it is unclear whether it is vmPFC loss per se, or the network-level consequences of this, that attenuates biases. Functional imaging studies in patients might potentially shed light on this in the future.

In summary, the results suggest that vmPFC may drive biases in healthy people. A patient with bilateral lesions won more than other participants did, coupled with more strategic betting and reduced biases, which were attenuated in unilateral patients too. vmPFC may bring contextual information to influence action, which may be suboptimal in some situations.