Neural substrates of approach-avoidance conflict decision-making

Abstract

Animal approach-avoidance conflict paradigms have been used extensively to operationalize anxiety, quantify the effects of anxiolytic agents, and probe the neural basis of fear and anxiety. Results from human neuroimaging studies support that a frontal-striatal-amygdala neural circuitry is important for approach-avoidance learning. However, the neural basis of decision-making is much less clear in this context. Thus, we combined a recently developed human approach-avoidance paradigm with functional magnetic resonance imaging (fMRI) to identify neural substrates underlying approach-avoidance conflict decision-making. Fifteen healthy adults completed the approach-avoidance conflict (AAC) paradigm during fMRI. Analyses of variance were used to compare conflict to nonconflict (avoid-threat and approach-reward) conditions and to compare level of reward points offered during the decision phase. Trial-by-trial amplitude modulation analyses were used to delineate brain areas underlying decision-making in the context of approach/avoidance behavior. Conflict trials as compared to the nonconflict trials elicited greater activation within bilateral anterior cingulate cortex, anterior insula, and caudate, as well as right dorsolateral prefrontal cortex (PFC). Right caudate and lateral PFC activation was modulated by level of reward offered. Individuals who showed greater caudate activation exhibited less approach behavior. On a trial-by-trial basis, greater right lateral PFC activation related to less approach behavior. Taken together, results suggest that the degree of activation within prefrontal-striatal-insula circuitry determines the degree of approach versus avoidance decision-making. Moreover, the degree of caudate and lateral PFC activation related to individual differences in approach-avoidance decision-making. Therefore, the approach-avoidance conflict paradigm is ideally suited to probe anxiety-related processing differences during approach-avoidance decision-making.

Keywords: anterior cingulate cortex; caudate; emotion; insula; prefrontal cortex; punishment; reward; striatum.

Figure 1

Decisional conditions included within the AAC paradigm. Avoid‐threat conditions (Part A) involve no point‐reward incentives but only the possibility of viewing a negative (indicated by a cloud) or positive (indicated by a sun) affective stimulus. Approach‐reward conditions (Part B) involve no threat of negative affective stimuli but only the possibility of obtaining reward points or no reward points (both paired with positive affective stimuli). During conflict conditions (Parts C–E), reward points (2, 4, or 6 point levels) are given only for the outcomes associated with a negative affective stimulus while the competing choice includes no points but a positive affective stimulus. The avatar starts out at different locations on the runway, counterbalanced within each of the condition types. The subject is asked to move the avatar (by pressing arrow keys on a keyboard) to a position that accurately reflects their preference between the two potential outcomes. The position in which they move the avatar determines the relative probability of each of the two outcomes occurring (Part E; 10/90%, 20/80%, 30/70%, 40/60%, 50/50%, and vice versa probabilities, corresponding to the nine potential avatar positions ranging from −4 to +4). Therefore, if they move their avatar to the middle, there is a 50% chance of each outcome occurring; if they moved all the way to one side, there is a 90% chance of the nearest outcome occurring, but still a 10% chance of the furthest outcome occurring, and so on. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Sequence of screens presented during one trial of the AAC task. A decisional phase is first presented for a maximum of 4 s. The affective stimulus phase consists of either a negative or positive affective image (from IAPS) [Lang et al., 2008] and a matched affective sound (from free source websites such as http://freesound.org and the IADS) [Bradley and Lang, 1999]. The affective stimulus phase lasts a total of 6 s. The reward phase consists of a screen displaying points earned on the current trial as well as the total points collected thus far on the task in combination with a reward‐related trumpet sound. The reward phase lasts a total of 2 s. An intertrial fixation averaging 6 s is displayed between trials. The AAC task consists of 18 trials of each condition type (displayed in Fig. 1), for a total of 90 trials. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Approach behavior during the AAC task. A +4 indicates the subjects moved the avatar all the way towards the NI and/or reward points. Approach behavior significantly differed between task conditions [F(4,56) = 60.75, P < 0.001). Post hoc tests revealed that approach behavior during conflict (2, 4, and 6‐point trials) significantly differed from avoid‐threat [t(14) = −8.60, P < 0.001] and approach‐reward [t(14) = 5.454, P < 0.001] conditions and that approach behavior during conflict increased significantly from 2‐point to 4‐point conditions [t(14) = −2.455, P = 0.028] but not from 4‐point to 6‐point conditions [t(14) = −0.833, P = 0.419].

Figure 4

Regions exhibiting greater activation for conflict than nonconflict conditions of the AAC. Conflict decision trials of the AAC were associated with greater activation than both approach‐reward and avoid‐threat decision trials within the (A) right ACC (BA 32; shown at x = 5), (B) right caudate (shown at y = 6), (C) right anterior insula (BA 13; shown at z=3), and (D) right dorsolateral prefrontal cortex (dlPFC; BA 9; shown at y = 8). As shown in the scatterplots, greater PSC to conflict conditions in the right caudate body (ρ = −0.62, P = .014) related to less average approach behavior for conflict trials of the AAC. Right dlPFC PSC related to self‐report of greater difficulty making decisions on the task (ρ = 0.77, P = 0.001). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

Regions exhibiting a relationship with approach behavior exhibited on individual trials. An amplitude‐modulated regressor (modulated by level of approach behavior on each trial) was used to identify regions relating to trial‐by‐trial approach behavior during conflict. Greater activation within (A) right lateral frontal [BA 6; 1216 mm³; t(14) = −3.53; x,y,z = 30, 6, 57; shown at x = 30] and (B) right middle/superior frontal (BA 10,46; 576 mm³; t(14) = −3.88; x,y,z = 39, 50, 15; shown at x = 38) related to less approach behavior. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]