The hippocampus is functionally connected to the striatum and orbitofrontal cortex during context dependent decision making

Abstract

Many of our everyday actions are only appropriate in certain situations and selecting the appropriate behavior requires that we use current context and previous experience to guide our decisions. The current study examined hippocampal functional connectivity with prefrontal and striatal regions during a task that required participants to make decisions based on the contextual retrieval of overlapping sequential representations. Participants learned four sequences comprised of six faces each. An overlapping condition was created by having two sequences with two identical faces as the middle images. A non-overlapping condition contained two sequences that did not share any faces between them. Hippocampal functional connectivity was assessed during the presentation period and at the critical choice, where participants had to make a contextually dependent decision. The left hippocampus showed significantly increased functional connectivity with dorsal and ventral striatum and anterior cingulate cortex during the presentation period of the overlapping compared to the non-overlapping condition after participants knew the sequences. At the critical choice point of the overlapping condition, the left hippocampus showed stronger functional connectivity with the orbitofrontal cortex. These functional connectivity results suggest that the hippocampus may play a role in decision making by predicting the possibilities of what might come next, allowing orbitofrontal and striatal regions to evaluate the expected choice options in order to make the correct action at the choice point.

Figure 1

Graphical representation of the overlapping and non-overlapping conditions. Each condition consisted of six faces represented by letters and numbers. The middle two faces of the two overlapping sequences were identical (X and Y). No faces were shared between the two non-overlapping sequences. Faces in the overlapping and non-overlapping sequences were always presented in the same order.

Figure 2

Behavioral paradigm. During the presentation phase, the first four faces of a sequence were shown paired with a blurred face for 4 second each. The presentation phase was followed by an 8 sec delay period where participants focused on a fixation dot. During the choice period, participants selected between two faces in order to complete the fifth and sixth elements of the sequence. The choice for the fifth element was termed the “critical choice” and the choice for the sixth element was termed the “final choice”. Face pairs during the choice phase were presented for 4 sec and response feedback indicated to participants whether or not they were correct. The choice phase was followed by a 6 sec inter-trial-interval (ITI). A 2 sec cue was shown after the ITI to indicate to participants if the upcoming trial was going to be a sequence trial (either overlapping or non-overlapping) or a random trial. Finally, a 2 sec prompt for the participant to “Get Ready” for the next trial was shown after the cue.

Figure 3

Behavioral results. (A) Mean percent accuracy at the critical choice point for the overlapping (OL) sequences (dark grey bars), non-overlapping (NOL) sequences (light grey bars) and random (RAN) conditions (white bars). (B) Mean reaction time in milliseconds at the critical choice point. (C) Mean run number at which participants reached the behavioral criteria and the data split into the learning and experienced phase for each condition. Asterisks indicate significance at p < 0.05.

Figure 4

Disambiguation related functional connectivity (overlapping > non-overlapping) with the left hippocampal seed region during the presentation period after participants knew the sequences. (A) Left hippocampal functional connectivity at the presentation phase with regions of the dorsal and ventral striatum (top panels and bottom left panel), anterior cingulate cortex (top left panel), posterior cingulate cortex (top right panel and bottom left panel), angular gyrus (bottom right panel), insula (bottom right panel) and middle frontal gyrus (bottom right panel). All images displayed on an average structural image of all 15 participants. (B) Results rendered on a whole brain. Red areas indicate regions showing significantly stronger functional connectivity with the left hippocampus during the overlapping condition compared to the non-overlapping condition during the presentation period after participants knew the sequences. All images displayed using p < 0.01 with 96 contiguous voxels. L = left hemisphere, R = right hemisphere

Figure 5

Disambiguation related functional connectivity with the left hippocampal seed region during the critical choice in the experienced phase of the task. (A) Left hippocampal functional connectivity with the orbitofrontal cortex (top left panel), rostral prefrontal cortex (top right panel), and supramarginal gyrus (bottom panels) when choosing between two overlapping choice options. (B) Results rendered on a whole brain. Red areas indicate regions showing significantly stronger functional connectivity with the left hippocampus during the overlapping condition compared to the non-overlapping condition at the critical choice point after participants knew the sequences. All images displayed using p < 0.01 with 96 contiguous voxels. L = left hemisphere, R = right hemisphere

Figure 6

Regions showing significant sequence related functional connectivity (non-overlapping > random) with the hippocampus. (A) Left hippocampus sequence related functional connectivity during the presentation phase while participants were learning the sequences with the ventral striatum, medial prefrontal cortex (MPFC) and the orbitofrontal cortex (OFC). (B) The top panels illustrate significant sequence related functional connectivity between the right hippocampus and the ventral striatum and rostral prefrontal cortex (RPFC) in the presentation phase while participants were learning the sequences. The bottom panels show medial prefrontal cortex (MPFC) and middle frontal gyrus (MFG) functional connectivity to the right hippocampus at the critical choice while participants were learning the sequences. (C) Regions showing significant functional connectivity with the right hippocampus at the critical choice after participants knew the sequences. All images displayed using p < 0.01 with 96 contiguous voxels. L = left hemisphere, R = right hemisphere