Retrieval of long-term episodic memories is characterized by synchronized neural activity between hippocampus and ventromedial prefrontal cortex (vmPFC), with additional evidence that vmPFC activity leads that of the hippocampus. It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. If this is the case, then a comparable interaction between the two brain regions should exist during the construction of novel scene imagery. To address this question, we leveraged the high temporal resolution of MEG to investigate the construction of novel mental imagery. We tasked male and female humans with imagining scenes and single isolated objects in response to one-word cues. We performed source-level power, coherence, and causality analyses to characterize the underlying interregional interactions. Both scene and object imagination resulted in theta power changes in the anterior hippocampus. However, higher theta coherence was observed between the hippocampus and vmPFC in the scene compared with the object condition. This interregional theta coherence also predicted whether imagined scenes were subsequently remembered. Dynamic causal modeling of this interaction revealed that vmPFC drove activity in hippocampus during novel scene construction. Additionally, theta power changes in the vmPFC preceded those observed in the hippocampus. These results constitute the first evidence in humans that episodic memory retrieval and scene imagination rely on similar vmPFC-hippocampus neural dynamics. Furthermore, they provide support for theories emphasizing similarities between both cognitive processes and perspectives that propose the vmPFC guides the construction of context-relevant representations in the hippocampus.SIGNIFICANCE STATEMENT Episodic memory retrieval is characterized by a dialog between hippocampus and ventromedial prefrontal cortex (vmPFC). It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. An ensuing prediction would be of a comparable interaction between the two brain regions during the construction of novel scene imagery. Here, we leveraged the high temporal resolution of MEG and combined it with a scene imagination task. We found that a hippocampal-vmPFC dialog existed and that it took the form of vmPFC driving the hippocampus. We conclude that episodic memory and scene imagination share fundamental neural dynamics and the process of constructing vivid, spatially coherent, contextually appropriate scene imagery is strongly modulated by vmPFC.

Questionnaires are used widely across psychology and permit valuable insights into a person's thoughts and beliefs, which are difficult to derive from task performance measures alone. Given their importance and widespread use, it is vital that questionnaires map onto the cognitive functions they purport to reflect. However, where performance on naturalistic tasks such as imagination, autobiographical memory, future thinking and navigation is concerned, there is a dearth of knowledge about the relationships between task performance and questionnaire measures. Questionnaires are also typically designed to probe a specific aspect of cognition, when instead researchers sometimes want to obtain a broad profile of a participant. To the best of our knowledge, no questionnaire exists that asks simple single questions about a wide range of cognitive functions. To address these gaps in the literature, we recruited a large sample of participants (n=217), all of whom completed a battery of widely used questionnaires and performed naturalistic tasks involving imagination, autobiographical memory, future thinking and navigation. We also devised a questionnaire that comprised simple single questions about the cognitive functions of interest. There were four main findings. First, imagination and navigation questionnaires reflected performance on their related tasks. Second, memory questionnaires were associated with autobiographical memory vividness and not internal (episodic) details. Third, imagery questionnaires were more associated with autobiographical memory vividness and future thinking than the questionnaires purporting to reflect these functions. Finally, initial exploratory analyses suggested that a broad profile of information can be obtained efficiently using a small number of simple single questions, and these modelled task performance comparably to established questionnaires in young, healthy adults. Overall, while some questionnaires can act as proxies for behaviour, the relationships between memory and future thinking tasks and questionnaires are more complex and require further elucidation.

Individual differences in scene imagination, autobiographical memory recall, future thinking and spatial navigation have long been linked with hippocampal structure in healthy people, although evidence for such relationships is, in fact, mixed. Extant studies have predominantly concentrated on hippocampal volume. However, it is now possible to use quantitative neuroimaging techniques to model different properties of tissue microstructure in vivo such as myelination and iron. Previous work has linked such measures with cognitive task performance, particularly in older adults. Here we investigated whether performance on scene imagination, autobiographical memory, future thinking and spatial navigation tasks was associated with hippocampal grey matter myelination or iron content in young, healthy adult participants. Magnetic resonance imaging data were collected using a multi-parameter mapping protocol (0.8 mm isotropic voxels) from a large sample of 217 people with widely-varying cognitive task scores. We found little evidence that hippocampal grey matter myelination or iron content were related to task performance. This was the case using different analysis methods (voxel-based quantification, partial correlations), when whole brain, hippocampal regions of interest, and posterior:anterior hippocampal ratios were examined, and across different participant sub-groups (divided by gender and task performance). Variations in hippocampal grey matter myelin and iron levels may not, therefore, help to explain individual differences in performance on hippocampal-dependent tasks, at least in young, healthy individuals.

We share data from N = 217 healthy adults (mean age 29 years, range 20-41; 109 females, 108 males) who underwent extensive cognitive assessment and neuroimaging to examine the neural basis of individual differences, with a particular focus on a brain structure called the hippocampus. Cognitive data were collected using a wide array of questionnaires, naturalistic tests that examined imagination, autobiographical memory recall and spatial navigation, traditional laboratory-based tests such as recalling word pairs, and comprehensive characterisation of the strategies used to perform the cognitive tests. 3 Tesla MRI data were also acquired and include multi-parameter mapping to examine tissue microstructure, diffusion-weighted MRI, T2-weighted high-resolution partial volume structural MRI scans (with the masks of hippocampal subfields manually segmented from these scans), whole brain resting state functional MRI scans and partial volume high resolution resting state functional MRI scans. This rich dataset will be of value to cognitive and clinical neuroscientists researching individual differences, real-world cognition, brain-behaviour associations, hippocampal subfields and more. All data are freely available on Dryad.

Marked disparities exist across healthy individuals in their ability to imagine scenes, recall autobiographical memories, think about the future and navigate in the world. The importance of the hippocampus in supporting these critical cognitive functions has prompted the question of whether differences in hippocampal grey matter volume could be one source of performance variability. Evidence to date has been somewhat mixed. In this study we sought to mitigate issues that commonly affect these types of studies. Data were collected from a large sample of 217 young, healthy adult participants, including whole brain structural MRI data (0.8 mm isotropic voxels) and widely-varying performance on scene imagination, autobiographical memory, future thinking and navigation tasks. We found little evidence that hippocampal grey matter volume was related to task performance in this healthy sample. This was the case using different analysis methods (voxel-based morphometry, partial correlations), when whole brain or hippocampal regions of interest were examined, when comparing different sub-groups (divided by gender, task performance, self-reported ability), and when using latent variables derived from across the cognitive tasks. Hippocampal grey matter volume may not, therefore, significantly influence performance on tasks known to require the hippocampus in healthy people. Perhaps only in extreme situations, as in the case of licensed London taxi drivers, are measurable ability-related hippocampus volume changes consistently exhibited.