The tipping point: Value differences and parallel dorsal–ventral frontal circuits gating human approach–avoidance behavior

Abstract

Excessive avoidance and diminished approach behavior are both prominent features of anxiety, trauma and stress related disorders. Despite this, little is known about the neuronal mechanisms supporting gating of human approach-avoidance behavior. Here, we used functional magnetic resonance imaging (fMRI) to track dorsal anterior cingulate and medial prefrontal (dACC/dmPFC) activation along an approach-avoidance continuum to assess sensitivity to competing appetitive and aversive contingencies and correspondence with behavior change. Behavioral and fMRI experiments were conducted using a novel approach-avoidance task where a monetary reward appeared in the presence of a conditioned stimulus (CS), or threat, that signaled increasing probability of unconditioned stimulus (US) delivery. Approach produced the reward or probabilistic US, while avoidance prevented US delivery, and across trials, reward remained fixed while the CS threat level varied unpredictably. Increasing the CS threat level (i.e., US probability) produced the desired approach-avoidance transition and inverted U-shaped changes in decision times, electrodermal activity and activation in pregenual ACC, dACC/dmPFC, striatum, anterior insula and inferior frontal regions. Conversely, U-shaped changes in activation were observed in dorsolateral and ventromedial prefrontal cortex and bimodal changes in the orbitofrontal and ventral hippocampus. These new results show parallel dorsal-ventral frontal circuits support gating of human approach-avoidance behavior where dACC/dmPFC signals inversely correlate with value differences between approach and avoidance contingencies while ventral frontal signals correlate with the value of predictable outcomes. Our findings provide an important bridge between basic research on brain mechanisms of value-guided decision-making and value-focused clinical theories of anxiety and related interventions.

Dorsal anterior cingulate and ventromedial prefrontal cortex have inverse roles in both foraging and economic choice

“…In both studies we find that the same regions of dACC that showed a positive relationship with foraging value for the range of RVFs in which the easier choice was to engage (i.e., ones that best approximated KBMR's design), show a robust negative association for the range of RVFs in which the easier choice is to forage. We note that in this respect our current study is the third rather than the second to show such an effect (see also Schlund et al, 2016). Kolling and colleagues (2014) examined dACC activity while subjects made risky choices in order to accumulate reward toward a target.…”

Animal to human translational paradigms relevant for approach avoidance conflict decision making

“…Neuroimaging findings of Aupperle et al (2011) and Schlund et al (2016) report very similar networks involved in processing conflict. Results highlight regions of the ACC, anterior insula, and caudate head in responding more to situations of high conflict, with Aupperle et al (2011) highlighting the potential importance of lateral frontal and caudate regions in avoidance behavior.…”

“…Results highlight regions of the ACC, anterior insula, and caudate head in responding more to situations of high conflict, with Aupperle et al (2011) highlighting the potential importance of lateral frontal and caudate regions in avoidance behavior. Interestingly, Aupperle et al (2011) reported right dlPFC to activate more during conflict (as compared to non-conflict situations), whereas Schlund et al (2016) reported left dlPFC to activate more during trials involving low conflict (i.e., either high threat or no threat). This discrepancy could be related to the lateralization of findings, as research reported above has found greater left dlPFC activation specifically to relate to approach tendencies, whereas right dlPFC activation relates to behavioral inhibition and avoidance tendencies.…”

“…Schlund et al (2016) recently developed a task aimed specifically at measuring approach-avoidance conflict behavior relevant to anxiety. This task has many similarities to the task developed by Aupperle et al (2011), but also some important differences.…”

“…Thus, while the choice/behavior is not associated with both a reward and punishment like in the AAC task and animal conflict paradigms, this method allows researchers to identify a “tipping” point at which the participant starts to avoid the potential threat. Using this paradigm, Schlund et al (2016) identified physiological and neural signatures that tracked level of conflict (greatest match in valuation between threat and reward outcomes) versus level of threat. Specifically, greater conflict (rather than threat) was associated with (a) slower reaction time, (b) increased skin conductance, and (c) greater activation within regions of the pregenual and dorsal ACC, dmPFC, caudate head, and anterior insula/IFG.…”