The rupture and repair of cooperation in borderline personality disorder

Abstract

To sustain or repair cooperation during a social exchange, adaptive creatures must understand social gestures and the consequences when shared expectations about fair exchange are violated by accident or intent. We recruited 55 individuals afflicted with borderline personality disorder (BPD) to play a multiround economic exchange game with healthy partners. Behaviorally, individuals with BPD showed a profound incapacity to maintain cooperation, and were impaired in their ability to repair broken cooperation on the basis of a quantitative measure of coaxing. Neurally, activity in the anterior insula, a region known to respond to norm violations across affective, interoceptive, economic, and social dimensions, strongly differentiated healthy participants from individuals with BPD. Healthy subjects showed a strong linear relation between anterior insula response and both magnitude of monetary offer received from their partner (input) and the amount of money repaid to their partner (output). In stark contrast, activity in the anterior insula of BPD participants was related only to the magnitude of repayment sent back to their partner (output), not to the magnitude of offers received (input). These neural and behavioral data suggest that norms used in perception of social gestures are pathologically perturbed or missing altogether among individuals with BPD. This game-theoretic approach to psychopathology may open doors to new ways of characterizing and studying a range of mental illnesses.

Fig. 1

Cooperation fails across rounds when individuals with BPD engage in a repeated exchange of trust. Among 38 healthy investors (gray) paired with healthy trustees (gray), investments were large and sustained across early (1 to 5) rounds and late (6 to 10) rounds of the game. However, among 55 healthy investors (gray) paired with 55 trustees with BPD (red), a decrease in investment level from early to late rounds of the game indicates a failure in cooperation across the iterated exchange. Mean percent invested and SEM are plotted.

Fig. 2

(A) Coaxing by trustees engenders trust from investors. Cooperation within the iterated trust game is expressed as high levels of investment combined with equitable sharing of investment returns (see fig. S2 for normative behavior). When cooperation falters (i.e., when investments are low), trustees can rebuild trust and cooperation by coaxing back higher and higher investment levels. In this schematic representation, the investor entrusts only a small portion of their endowment ($5 of $20 points) to their partner. The $15 received by the trustee is far less than the $60 that would have been received if the investor had sent the entire endowment. Thus, in order to maximize their gains, a trustee must induce cooperation in a repeated exchange. The trustee can coax back trust from their partner by repaying a large proportion of the tripled investment–signaling their own trustworthiness and, thus, eliciting larger subsequent investments. Conversely, if the trustee does not coax and instead keeps a large proportion of the tripled investment, the investor is likely to invest less on subsequent rounds and cooperation will continue to devolve. (B) Coaxing pays off. The effect of such coaxing is summarized in the effect of repayment on investments in subsequent rounds among healthy subjects. This analysis is restricted to low investments (all rounds with investments <$5). Blue bars depict mean ± SE investment level following small repayments (repayment less than one-third of the tripled investment; “no coax” condition); green bars depict investment level following large repayments (more than or equal to one-third; “coax” condition). The analysis indicates that coaxing elicits larger investments in rounds following coaxing behavior (green) than for rounds following no coaxing (blue). Note that the coaxing-related increase in investment persists across rounds, such that a large repayment in the current round earns larger investment up to four rounds into the future. (C) BPD subjects coax less. Healthy trustees are twice as likely as BPD trustees to coax when cooperation between players is low. Specifically, healthy trustees are more likely to make a large repayment (≥ investment amount) after having received a small investment (≤$5). Conversely, BPD trustees are more likely to make a small repayment (< investment amount) after receiving a small investment. The y axis indicates the proportion of exchanges that trustees repay more than or equal to the investment amount after receiving a small investment (≤$5).

Fig. 3

Response of 38 healthy trustee brains and 55 BPD trustee brains to level of cooperation. (Top) Results of both between- and within-group GLM analyses identified cortical regions with greater response to small investments (I ≤ $5) relative to large investments (I > $10). All significant voxels are conservatively corrected using false-discovery rate procedures to the P < 0.05 level in yellow; P < 0.10 in orange (see tables S3 to S5). (Bottom) Percent change in hemodynamic signal was averaged from the 115 most significant voxels identified in the group-level GLM (top left and table S3) during the 4- to 8-s period following the revelation of investment. The means ± SE of the resulting signal are plotted in $4 bins. Responses in bilateral anterior insula in healthy trustees scale strongly and negatively with the size of investment (r = −0.97; bottom middle). In contrast, similar analyses in individuals with BPD showed no such relation.

Fig. 4

Diminished relation of insula activity to investment level is not attributable to medication status or income level in BPD trustees. ROI analyses within subsamples of BPD trustees were performed as described in Fig. 3. The systematic negative relation of investment level to bilateral anterior insula activity seen in healthy controls is absent in both medicated and unmedicated BPD trustees, as well as in BPD trustees matched to the income level of the control group.

Fig. 5

Both healthy and BPD trustees exhibit a systematic negative relation of repayment level and bilateral anterior insula activity during their decision to repay. ROI analyses were performed using bilateral anterior insula voxels identified in the between-group analysis illustrated in Fig. 3 and used in the ROI analyses of Figs. 3 and 4. To investigate whether the insula activity also scales with trustee responses to norm violations, insula activity during trustee decisions is plotted by repayment level. Both healthy and BPD trustees show a strong negative relation between activity and repayment level. As trustees repaid more than 60% of the tripled investment in only ~ 7% of rounds, high repayment rounds are excluded from this analysis.

Fig. 6

Behavioral and self-report levels of trust indicate perturbed social norms among individuals with BPD. (Left) Individuals with BPD report lower trait levels of trust using a self-report measure [Interpersonal Trust Scale (55)]. (Right) Individuals with BPD repay less than the healthy group, which indicate lower levels of trust within the exchange game (also see fig. S2).