The Neural Representation of Prospective Choice during Spatial Planning and Decisions

Abstract

We are remarkably adept at inferring the consequences of our actions, yet the neuronal mechanisms that allow us to plan a sequence of novel choices remain unclear. We used functional magnetic resonance imaging (fMRI) to investigate how the human brain plans the shortest path to a goal in novel mazes with one (shallow maze) or two (deep maze) choice points. We observed two distinct anterior prefrontal responses to demanding choices at the second choice point: one in rostrodorsal medial prefrontal cortex (rd-mPFC)/superior frontal gyrus (SFG) that was also sensitive to (deactivated by) demanding initial choices and another in lateral frontopolar cortex (lFPC), which was only engaged by demanding choices at the second choice point. Furthermore, we identified hippocampal responses during planning that correlated with subsequent choice accuracy and response time, particularly in mazes affording sequential choices. Psychophysiological interaction (PPI) analyses showed that coupling between the hippocampus and rd-mPFC increases during sequential (deep versus shallow) planning and is higher before correct versus incorrect choices. In short, using a naturalistic spatial planning paradigm, we reveal how the human brain represents sequential choices during planning without extensive training. Our data highlight a network centred on the cortical midline and hippocampus that allows us to make prospective choices while maintaining initial choices during planning in novel environments.

Human back-tracking behaviour is associated with suppression of default-mode region activity and enhanced dorsal anterior cingulate activity

“…Across both externally driven (Detours, False Shortcuts) and internally driven (Backtracking) route re-evaluation events we found increased activation in the dorso-medial PFC, an area that has been implicated in various contexts including: hierarchical planning (Balaguer, Spiers, Hassabis, & Summerfield, 2016), high planning demand decisions (Kaplan et al, 2017), and model updating, irrespective of difficulty or simple error-related signalling (Kolling et al, 2016;O'Reilly et al, 2013). However, we found activation in the dorsal anterior cingulate cortex (dACC) was much more pronounced during Back-tracking, possibly reflecting stronger engagement of planning and error signals when participants spontaneously realized that they were on a sub-optimal path.…”

Internally generated hippocampal sequences as a vantage point to probe future‐oriented cognition

“…Perhaps understanding how SWR sequences mesh episodes coherently (e.g., adjacent trajectories but not separated ones) may shed light on how human episodic constructive memory works (e.g., meshing memories of oneself at in the grandmother's house and of oneself at a past children's party to imagine how a children's party at the grandmother's house would be). Progress in the field may come from studies that directly probe sequential activity resembling SWR or theta sequences during human cognitive processing, possibly designed to test (and disentangle) alternative computational models.…”

Planning and navigation as active inference

“…2017a). Interestingly, we observed two anterior prefrontal responses to demanding choices at the second choice point: one in rostro-dorsal medial prefrontal cortex (rd-mPFC)—that was also sensitive to demanding initial choices—and another in lateral frontopolar cortex—that was only engaged by demanding choices at the second choice point.…”