Elsevier

Neuropsychologia

Volume 75, August 2015, Pages 265-273
Neuropsychologia

Sex-related functional asymmetry of the ventromedial prefrontal cortex in regard to decision-making under risk and ambiguity

https://doi.org/10.1016/j.neuropsychologia.2015.06.015Get rights and content

Highlights

  • There are sex differences in vmPFC laterality in decision making.

  • Men with right-sided, women with left-sided vmPFC damage show lower aversion to risk.

  • Men with right-sided, women with left-sided vmPFC damage show less ambiguity aversion.

  • Neural substrates supporting similar behavioral performance can differ between sexes.

Abstract

Previous work has provided preliminary indication of sex-related functional asymmetry of the ventromedial prefrontal cortex (vmPFC) in social and emotional functions and complex decision-making. Findings have been inconsistent, and based on small numbers of patients. Given the rarity of these neurological cases, replicable results across studies are important to build evidence for sex-related functional asymmetry of the vmPFC. Here we used a sample of sixteen neurological patients with unilateral damage to the left or right vmPFC and examined differences between men and women on a task that probed decision-making under risk or decision-making under ambiguity. We found that men with right-hemisphere vmPFC damage and women with left-hemisphere vmPFC damage demonstrated significantly reduced aversion to risk and ambiguity. Men with damage to the left vmPFC and women with damage to the right vmPFC showed aversion to risk and ambiguity comparable to participants with left or right-sided brain damage outside the vmPFC, and to comparison participants without brain damage. Our results add to previous findings of sex-related functional asymmetry of the vmPFC in decision-making. Our study also replicates findings of no observable behavioral differences between men and women without neurological damage on tests of decision-making. This pattern of neurobiological divergence but behavioral convergence between men and women may reflect a complex interplay of neuroendocrine, developmental, and psychosocial factors.

Introduction

Studies of neurological and cognitive differences between men and women are often sources of both fascination and controversy. It is commonly accepted that there are sex-related differences in structural and functional brain organization in both animals and humans (Cahill, 2006). However, the extent of the differences and the degree to which these neural differences impact behavior vary between the brain areas and behaviors studied. Classically observed differences between men and women on verbal and spatial behaviors have been discussed at length (see Kimura, 1996). However, other cognitive functions such as naming and emotional memory show no sex-related differences at the behavioral level despite clear distinctions between men and women at the neural level (Grabowski et al., 2003, Piefke et al., 2005).

In the domain of decision-making, evidence is less clear for sex-related differences in neural organization resulting in observed behavioral differences. While decision-making can encompass a wide array of distinct behavior, of particular interest are decisions under risk (where the probability of all outcomes are known), and ambiguity (where the probability of outcomes are unknown). Research from behavioral economics has indicated that women show a greater aversion than men to decision-making under risk as well as ambiguity (Borghans et al., 2009, Charness and Gneezy, 2012, Powell and Ansic, 1997), while other studies from clinical psychology and neuroscience have found no differences between men and women on other tasks of risky and ambiguous decision-making (Deakin et al., 1999, Gardner and Steinberg, 2005, Lee et al., 2009, Lighthall et al., 2009, Starcke et al., 2008, van den Bos et al., 2013).

The ventromedial prefrontal cortex (vmPFC), along with other areas, has been identified as a critical neural area for decision-making (Damasio, 1994, Sanfey, 2007). Previous studies have found evidence of a ‘reversed asymmetry’ between men and women with damage to the vmPFC, such that men with right-sided vmPFC damage, and women with left-sided vmPFC damage, demonstrate deficits in social-emotional processing and performance on the Iowa gambling task (IGT), a measure of naturalistic decision-making (Bechara et al., 1994, Tranel et al., 2002, Tranel et al., 2005). This lesion evidence has been complemented by neuroimaging research, which has shown greater right prefrontal activation in men, and greater left prefrontal activation in women during the IGT (Bolla et al., 2004). However, the IGT is a complex measure of decision-making with elements of both decision-making under risk and ambiguity, preventing easy decomposition into discrete cognitive constructs (Schonberg et al., 2011). Closer study of the components of decision-making affected by sex-related, functional asymmetry of the vmPFC is necessary to better understand which cognitive elements are different between men and women. The goal of the current study is to add to previous findings of sex-related, functional asymmetry of the prefrontal cortex, using a task that allows us to examine the decision-making subcomponents of risk and ambiguity in a more conclusive manner. Based on previous work, we predict that men with right-sided, and women with left-sided vmPFC lesions will show deficits in decision-making under risk and ambiguity, while men with left-sided and women with right-sided vmPFC lesions, as well as men and women damage outside vmPFC, will not show deficits in decision-making.

Section snippets

Participants

Participants with focal, unilateral damage to the vmPFC (n=16, 9 men/7 women, 10 right-sided/6 left-sided) were recruited from the Patient Registry of the Division of Cognitive Neuroscience at the University of Iowa (Iowa City, IA). The demographic and neuropsychological characteristics of these 16 participants are presented in Table 1. Brain damage was acquired in adulthood for all vmPFC participants with the exception of 2046, 2097, and 2517, whose damage occurred during development (prior to

Results

We examined vmPFC, BDC, and NC behavior in the Card Deck condition, using univariate ANOVAs to test the interaction of sex, lesion side, and group on risk and ambiguity aversion, as well as expected value preference. The ANOVA tests revealed significant three-way interactions between sex, laterality and lesion location for risk aversion [F(1,176)=7.31, p=0.01], and ambiguity aversion [F(1,176)=8.36, p=0.004]. The three-way interaction for expected value preference was nonsignificant [F

Discussion

On a task of decision-making under risk and ambiguity, we observed significant deficits in risk and ambiguity aversion between men with right-sided and women with left-sided damage to the ventromedial prefrontal cortex (respectively). Men with vmPFC damage to the left hemisphere and women with vmPFC damage to the right hemisphere show normal risk and ambiguity aversion, as do brain-damaged comparison participants of both sexes with damage outside the vmPFC. This evidence is in line with

Conclusions

The current study replicated and extended previous reports of sex-related asymmetry of the ventromedial prefrontal cortex (Gaznick et al., 2014, Tranel et al., 2005), such that men with right-sided and women with left sided damage show similar deficits in decision-making under risk and ambiguity. While this dissociation provides additional evidence of differences in functional organization of brain regions important for decision-making, this study also supports findings of similarities in

Funding

This work was supported by the National Institute on Drug Abuse [R01 DA022549 to D.T.] and the National Institute of Neurological Disorders and Stroke, USA [P01 NS19632 to D.T.; F31 NS086254 to M.S.], by a McDonnell Foundation Collaborative Action Award [#220020387 to D.T.], and NSERC (Natural Sciences and Engineering Research Council of Canada), Canada PGS-D (Postgraduate Scholarship-Doctoral program) and CIHR (Canadian Institutes of Health Research) PDF (Postdoctoral Fellowship) [to T.K.]

Acknowledgments

The authors thank Joel Bruss for assistance with neuroanatomical registration and creation of overlap maps, and Matthew Calamia for consultation on statistical analyses.

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