Do questionnaires reflect their purported cognitive functions?

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

Neural processes underpinning episodic memory

Episodic memory is the memory for our personal past experiences. Although numerous functional magnetic resonance imaging (fMRI) studies investigating its neural basis have revealed a consistent and distributed network of associated brain regions, surprisingly little is known about the contributions individual brain areas make to the recollective experience. In this thesis I address this fundamental issue by employing a range of different experimental techniques including neuropsychological testing, virtual reality environments, whole brain and high spatial resolution fMRI, and multivariate pattern analysis. Episodic memory recall is widely agreed to be a reconstructive process, one that is known to be critically reliant on the hippocampus. I therefore hypothesised that the same neural machinery responsible for reconstruction might also support ‘constructive’ cognitive functions such as imagination. To test this proposal, patients with focal damage to the hippocampus bilaterally were asked to imagine new experiences and were found to be impaired relative to matched control participants. Moreover, driving this deficit was a lack of spatial coherence in their imagined experiences, pointing to a role for the hippocampus in binding together the disparate elements of a scene. A subsequent fMRI study involving healthy participants compared the recall of real memories with the construction of imaginary memories. This revealed a fronto-temporo-parietal network in common to both tasks that included the hippocampus, ventromedial prefrontal, retrosplenial and parietal cortices. Based on these results I advanced the notion that this network might support the process of ‘scene construction’, defined as the generation and maintenance of a complex and coherent spatial context. Furthermore, I argued that this scene construction network might underpin other important cognitive functions besides episodic memory and imagination, such as navigation and thinking about the future. It is has been proposed that spatial context may act as the scaffold around which episodic memories are built. Given the hippocampus appears to play a critical role in imagination by supporting the creation of a rich coherent spatial scene, I sought to explore the nature of this hippocampal spatial code in a novel way. By combining high spatial resolution fMRI with multivariate pattern analysis techniques it proved possible to accurately determine where a subject was located in a virtual reality environment based solely on the pattern of activity across hippocampal voxels. For this to have been possible, the hippocampal population code must be large and non-uniform. I then extended these techniques to the domain of episodic memory by showing that individual memories could be accurately decoded from the pattern of activity across hippocampal voxels, thus identifying individual memory traces. I consider these findings together with other recent advances in the episodic memory field, and present a new perspective on the role of the hippocampus in episodic recollection. I discuss how this new (and preliminary) framework compares with current prevailing theories of hippocampal function, and suggest how it might account for some previously contradictory data

Verbal paired associates and the hippocampus: The role of scenes

It is widely agreed that patients with bilateral hippocampal damage are impaired at binding pairs of words together. Consequently, the verbal paired associates (VPA) task has become emblematic of hippocampal function. This VPA deficit is not well understood and is particularly difficult for hippocampal theories with a visuospatial bias to explain (e.g., cognitive map and scene construction theories). Resolving the tension among hippocampal theories concerning the VPA could be important for leveraging a fuller understanding of hippocampal function. Notably, VPA tasks typically use high imagery concrete words and so conflate imagery and binding. To determine why VPA engages the hippocampus, we devised an fMRI encoding task involving closely matched pairs of scene words, pairs of object words, and pairs of very low imagery abstract words. We found that the anterior hippocampus was engaged during processing of both scene and object word pairs in comparison to abstract word pairs, despite binding occurring in all conditions. This was also the case when just subsequently remembered stimuli were considered. Moreover, for object word pairs, fMRI activity patterns in anterior hippocampus were more similar to those for scene imagery than object imagery. This was especially evident in participants who were high imagery users and not in mid and low imagery users. Overall, our results show that hippocampal engagement during VPA, even when object word pairs are involved, seems to be evoked by scene imagery rather than binding. This may help to resolve the issue that visuospatial hippocampal theories have in accounting for verbal memory

The pre/parasubiculum: a hippocampal hub for scene-based cognition?

Internal representations of the world in the form of spatially coherent scenes have been linked with cognitive functions including episodic memory, navigation and imagining the future. In human neuroimaging studies, a specific hippocampal subregion, the pre/parasubiculum, is consistently engaged during scene-based cognition. Here we review recent evidence to consider why this might be the case. We note that the pre/ parasubiculum is a primary target of the parieto-medial temporal processing pathway, it receives integrated information from foveal and peripheral visual inputs and it is contiguous with the retrosplenial cortex. We discuss why these factors might indicate that the pre/parasubiculum has privileged access to holistic representations of the environment and could be neuroanatomically determined to preferentially process scenes

Characterizing Strategy Use During the Performance of Hippocampal-Dependent Tasks

Recalling the past, thinking about the future, and navigating in the world are linked with a brain structure called the hippocampus. Precisely, how the hippocampus enables these critical cognitive functions is still debated. The strategies people use to perform tasks associated with these functions have been under-studied, and yet, such information could augment our understanding of the associated cognitive processes and neural substrates. Here, we devised and deployed an in-depth protocol to examine the explicit strategies used by 217 participants to perform four naturalistic tasks widely acknowledged to be hippocampal-dependent, namely, those assessing scene imagination, autobiographical memory recall, future thinking, and spatial navigation. In addition, we also investigated strategy use for three laboratory-based memory tasks, one of which is held to be hippocampal-dependent – concrete verbal paired associates (VPA) – and two tasks, which are likely hippocampal-independent – abstract VPA and the dead or alive semantic memory test. We found that scene visual imagery was the dominant strategy not only when mentally imagining scenes, but also during autobiographical memory recall, when thinking about the future and during navigation. Moreover, scene visual imagery strategies were used most frequently during the concrete VPA task, whereas verbal strategies were most prevalent for the abstract VPA task and the dead or alive semantic memory task. The ubiquity of specifically scene visual imagery use across a range of tasks may attest to its, perhaps underappreciated, importance in facilitating cognition, while also aligning with perspectives that emphasize a key role for the hippocampus in constructing scene imagery

Scene construction impairments in Alzheimer's disease – A unique role for the posterior cingulate cortex

Episodic memory dysfunction represents one of the most prominent and characteristic clinical features of patients with Alzheimer's disease (AD), attributable to the degeneration of medial temporal and posterior parietal regions of the brain. Recent studies have demonstrated marked impairments in the ability to envisage personally relevant events in the future in AD. It remains unclear, however, whether AD patients can imagine fictitious scenes free from temporal constraints, a process that is proposed to rely fundamentally upon the integrity of the hippocampus. The objective of the present study was to investigate the capacity for atemporal scene construction, and its associated neural substrates, in AD. Fourteen AD patients were tested on the scene construction task and their performance was contrasted with 14 age- and education-matched healthy older Control participants. Scene construction performance was strikingly compromised in the AD group, with significant impairments evident for provision of contextual details, spatial coherence, and the overall richness of the imagined experience. Voxel-based morphometry analyses based on structural MRI revealed significant associations between scene construction capacity and atrophy in posterior parietal and lateral temporal brain structures in AD. In contrast, scene construction performance in Controls was related to integrity of frontal, parietal, and medial temporal structures, including the parahippocampal gyrus and posterior hippocampus. The posterior cingulate cortex (PCC) emerged as the common region implicated for scene construction performance across participant groups. Our study highlights the importance of regions specialised for spatial and contextual processing for the construction of atemporal scenes. Damage to these regions in AD compromises the ability to construct novel scenes, leading to the recapitulation of content from previously experienced events

Building Mental Experiences: From Scenes to Events

Mental events are central to everyday cognition, be it our continuous perception of the world, recalling autobiographical memories, or imagining the future. Little is known about the fine-grained temporal dynamics of these processes. Given the apparent predominance of scene imagery across cognition, in this thesis I used magnetoencephalography to investigate whether and how activity in the hippocampus and ventromedial prefrontal cortex (vmPFC) supports the mental construction of scenes and the events to which they give rise. In the first experiment, participants gradually imagined scenes and also closely matched non-scene arrays; this allowed me to assess whether any brain regions showed preferential responses to scene imagery. The anterior hippocampus and vmPFC were particularly engaged by the construction of scene imagery, with the vmPFC driving hippocampal activity. In the second experiment, I found that certain objects – those that were space-defining – preferentially engaged the vmPFC and superior temporal gyrus during scene construction, providing insight into how objects affect the creation of scene representations. The third experiment involved boundary extension during scene perception, permitting me to examine how single scenes might be prepared for inclusion into events. I observed changes in evoked responses just 12.5-58 ms after scene onset over fronto-temporal sensors, with again the vmPFC exerting a driving influence on other brain regions, including the hippocampus. In the final experiment, participants watched brief movies of events built from a series of scenes or non-scene patterns. A difference in evoked responses between the two event types emerged during the first frame of the movies, the primary source of which was shown to be the hippocampus. The enduring theme of the results across experiments was scene-specific engagement of the hippocampus and vmPFC, with the latter being the driving influence. Overall, this thesis provides insights into the neural dynamics of how scenes are built, made ready for inclusion into unfolding mental episodes, and then linked to produce our seamless experience of the world

Release of cognitive and multimodal MRI data including real-world tasks and hippocampal subfield segmentations

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

Which Way Was I Going? Contextual Retrieval Supports the Disambiguation of Well Learned Overlapping Navigational Routes

Groundbreaking research in animals has demonstrated that the hippocampus contains neurons that distinguish betweenoverlapping navigational trajectories. These hippocampal neurons respond selectively to the context of specific episodes despite interference from overlapping memory representations. The present study used functional magnetic resonanceimaging in humans to examine the role of the hippocampus and related structures when participants need to retrievecontextual information to navigate well learned spatial sequences that share common elements. Participants were trained outside the scanner to navigate through 12 virtual mazes from a ground-level first-person perspective. Six of the 12 mazes shared overlapping components. Overlapping mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required the retrieval of contextual information relevant to thecurrent navigational episode. Results revealed greater activation during the successful navigation of the overlapping mazes compared with the non-overlapping mazes in regions typically associated with spatial and episodic memory, including thehippocampus, parahippocampal cortex, and orbitofrontal cortex. When combined with previous research, the current findings suggest that an anatomically integrated system including the hippocampus, parahippocampal cortex, and orbitofrontal cortexis critical for the contextually dependent retrieval of well learned overlapping navigational routes

Constructing, Perceiving, and Maintaining Scenes: Hippocampal Activity and Connectivity.

In recent years, evidence has accumulated to suggest the hippocampus plays a role beyond memory. A strong hippocampal response to scenes has been noted, and patients with bilateral hippocampal damage cannot vividly recall scenes from their past or construct scenes in their imagination. There is debate about whether the hippocampus is involved in the online processing of scenes independent of memory. Here, we investigated the hippocampal response to visually perceiving scenes, constructing scenes in the imagination, and maintaining scenes in working memory. We found extensive hippocampal activation for perceiving scenes, and a circumscribed area of anterior medial hippocampus common to perception and construction. There was significantly less hippocampal activity for maintaining scenes in working memory. We also explored the functional connectivity of the anterior medial hippocampus and found significantly stronger connectivity with a distributed set of brain areas during scene construction compared with scene perception. These results increase our knowledge of the hippocampus by identifying a subregion commonly engaged by scenes, whether perceived or constructed, by separating scene construction from working memory, and by revealing the functional network underlying scene construction, offering new insights into why patients with hippocampal lesions cannot construct scenes