Differentiable Processing of Objects, Associations, and Scenes within the Hippocampus

Abstract

The hippocampus is known to be important for a range of cognitive functions, including episodic memory, spatial navigation, and thinking about the future. However, researchers have found it difficult to agree on the exact nature of this brain structure's contribution to cognition. Some theories emphasize the role of the hippocampus in associative processes. Another theory proposes that scene construction is its primary role. To directly compare these accounts of hippocampal function in human males and females, we devised a novel mental imagery paradigm where different tasks were closely matched for associative processing and mental construction, but either did or did not evoke scene representations, and we combined this with high-resolution functional MRI. The results were striking in showing that different parts of the hippocampus, along with distinct cortical regions, were recruited for scene construction or nonscene-evoking associative processing. The contrasting patterns of neural engagement could not be accounted for by differences in eye movements, mnemonic processing, or the phenomenology of mental imagery. These results inform conceptual debates in the field by showing that the hippocampus does not seem to favor one type of process over another; it is not a story of exclusivity. Rather, there may be different circuits within the hippocampus, each associated with different cortical inputs, which become engaged depending on the nature of the stimuli and the task at hand. Overall, our findings emphasize the importance of considering the hippocampus as a heterogeneous structure, and that a focus on characterizing how specific portions of the hippocampus interact with other brain regions may promote a better understanding of its role in cognition.SIGNIFICANCE STATEMENT The hippocampus is known to be important for a range of cognitive functions, including episodic memory, spatial navigation, and thinking about the future. However, researchers have found it difficult to agree on the exact nature of this brain structure's contribution to cognition. Here we used a novel mental imagery paradigm and high-resolution functional MRI to compare accounts of hippocampal function that emphasize associative processes with a theory that proposes scene construction as a primary role. The results were striking in showing that different parts of the hippocampus, along with distinct cortical regions, were recruited for scene construction or nonscene-evoking associative processing. We conclude that a greater emphasis on characterizing how specific portions of the hippocampus interact with other brain regions may promote a better understanding of its role in cognition.

Differences in functional connectivity along the anterior-posterior axis of human hippocampal subfields

“…Multiple elements of our results, however, clearly show that the pre/parasubiculum and subiculum proper have different patterns of FC. Together with the recent observation that even different regions of the pre/parasubiculum may facilitate distinct forms of mental imagery (Dalton et al, 2018), the current findings provide persuasive evidence that neuroimaging investigations of the hippocampus should, at the very least, differentiate between the pre/parasubiculum and the subiculum proper when investigating contributions of this complex region to human cognition. Indeed, Insausti et al (2017) recently suggested that the concept of a 'subicular cortex' may be incorrect considering it combines the differentiable subicular allocortex (comprising 3 layers) and the pre/parasubicular periallocortex (comprising 6 layers).…”

“…We have consistently observed a functional cluster in the medial hippocampus which extends across this demarcation point in tasks relating to scene-based cognition (Dalton et al, 2018;Zeidman et al, 2015a,b;Zeidman and Maguire, 2016). Hence, we believe that this portion of the hippocampus may represent a functional module which, when utilising the uncus-based anatomical demarcation point, would potentially be split between two separate ROIs.…”

Content-based dissociation of hippocampal involvement in prediction

“…Recent theories of the hippocampus suggest that it performs general-purpose computations independent of stimulus contents (20). Alternatively, it has been suggested that the nature of stimuli, especially their complexity, is a crucial factor in determining whether hippocampus and MTL are involved in a given perceptual task (31,42). The current study addresses these hypotheses by revealing that predictions about complex shapes and simple grating orientations evoked qualitatively different representations in the hippocampus.…”

Interplay of the long axis of the hippocampus and ventromedial prefrontal cortex in schema‐related memory retrieval

“…Consistent with our results, Webb et al () investigated subsequent memory effects for objects that were encoded either in congruent or incongruent scenes and found increased aHPC activation for schema‐related recollection. Human fMRI studies have also suggested that activation in the aHPC is associated with constructing mental representations of scenes (Dalton, Zeidman, McCormick, & Maguire, ; Zeidman & Maguire, ). Taken together, the results support our hypothesis that the schematic context can be used to facilitate retrieving schema‐related information, and the anterior hippocampus is involved in this process.…”

“…Human fMRI studies have also suggested that activation in the aHPC is associated with constructing mental representations of scenes (Dalton, Zeidman, McCormick, & Maguire, 2018;Zeidman & Maguire, 2016).…”