Hippocampus Prospective Representation of Navigational Goals

 

Science  10 Jun 2016: Vol. 352, Issue 6291, pp. 1323-1326

Prospective representation of navigational goals in the human hippocampus

Thackery I. Brown, et.al.

Department of Psychology, Stanford University, Stanford, CA, USA.

Department of Psychology, San Jose State University, San Jose, CA, USA.

Department of Psychology, New York University, New York, NY, USA.

Department of Psychology, University of California–Berkeley, Berkeley, CA, USA.

Department of Communication, Stanford University, Stanford, CA, USA.

Neurosciences Program, Stanford University, Stanford, CA, USA.

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Mental representation of the future is a fundamental component of goal-directed behavior. Computational and animal models highlight prospective spatial coding in the hippocampus, mediated by interactions with the prefrontal cortex, as a putative mechanism for simulating future events. Using whole-brain high-resolution functional magnetic resonance imaging and multi-voxel pattern classification, we tested whether the human hippocampus and interrelated cortical structures support prospective representation of navigational goals. Results demonstrated that hippocampal activity patterns code for future goals to which participants subsequently navigate, as well as for intervening locations along the route, consistent with trajectory-specific simulation. The strength of hippocampal goal representations covaried with goal-related coding in the prefrontal, medial temporal, and medial parietal cortex. Collectively, these data indicate that a hippocampal-cortical network supports prospective simulation of navigational events during goal-directed planning.

Prospective thought and the simulation of future experiences are fundamental for planning how to best achieve immediate and longer-term goals. Prospection is theorized to rely on neural mechanisms that underlie episodic memory, drawing on declarative memory for distinct events to flexibly simulate future experiences and outcomes. The hippocampus subserves episodic retrieval of goal-relevant spatial sequences in rodents and humans and plays a central role in models of goal-directed navigation and episodic memory. In rodents, hippocampal “place cells” exhibit prospective sequential firing along navigational routes during planning that reflects current goals. Prospective firing may support reinstatement of the multifeatural representations of spatial contexts in a broader network underlying prospection and goal coding [including the medial temporal lobe (MTL), retrosplenial complex (RSC), and ventral striatum (VS)]. Prospective simulation may also rely on hippocampal interactions with the prefrontal cortex (PFC), which may provide cognitive control machinery through which mnemonic details are flexibly accessed and combined into the formulation of future route plans. A fundamental question in human cognitive neuroscience is whether the hippocampus and its functional interactions support flexible prospective representation of spatial trajectories during goal-directed planning.

Although human hippocampal neurons demonstrate location- and goal-related responses that can be reinstated during retrieval, noninvasive quantification of the neural representation of spatial information in humans is a challenge. Functional magnetic resonance imaging (fMRI) has revealed distance-to-goal and grid cell–like response coding in the human hippocampus and entorhinal cortex. Measurement of purely place cell–based location codes may not be feasible with fMRI; however, it may be possible to quantify episodic retrieval of a distributed multifeatural engram of a spatial context. Multivariate fMRI approaches have demonstrated that distributed patterns in the hippocampus, MTL cortex, and RSC carry representational information about environmental features, locations, and the direction to a goal. However, direct evidence that this hippocampal-cortical network supports prospective goal coding during route planning in humans has yet to be shown.

We used whole-brain high-resolution fMRI (hr-fMRI; 1.6-mm isotropic voxels) to simultaneously record fine-grained pattern information from the human hippocampus and a core network of anatomically and functionally interconnected regions putatively involved in goal coding and prospection.

To plan future behavior, humans and animals must be able to represent goals within an environment, as well as to retrieve potential means of reaching these goals. Our data indicate that the hippocampus, interacting with a functionally linked neocortical network (MTL cortex, RSC, and OFC), provides a mechanism for such mental simulation. In particular, our data encompass several important advances: We demonstrate that the human hippocampus contributes to goal-directed navigation, in part through representing future goal states as well as features of the current location, and, critically, we provide evidence that such prospective retrieval includes episodic simulation of the intended route. Although it remains to be seen whether similar coding and computations occur in more complex large-scale environments, such as those that humans traverse in daily life, this work bridges the prospective coding of navigational goals in the human hippocampus with related findings in rodents. Moreover, models of episodic memory and navigation emphasize the importance of hippocampal-prefrontal interactions for representing navigational events and route planning. Our results provide evidence for an association between prospective hippocampal representations and putative planning processes in the FPC. More broadly, these findings illuminate the mechanistic role of the hippocampus, along with an extended MTL cortex, orbitofrontal, and retrosplenial network, in memory-guided simulation of future events. This network, along with the FPC, links look-ahead–like processes with goal-directed planning, which together enable humans to think prospectively.

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