Elsevier

Cortex

Volume 120, November 2019, Pages 588-602
Cortex

Brain activation in highly superior autobiographical memory: The role of the precuneus in the autobiographical memory retrieval network

https://doi.org/10.1016/j.cortex.2019.02.020Get rights and content

Abstract

This is the first study to examine functional brain activation in a single case of Highly Superior Autobiographical Memory (HSAM) who shows no sign of obsessive compulsive disorder (OCD). While previous work has documented the existence of HSAM, information about brain areas involved in this exceptional form of memory for personal events relies on structural and resting state connectivity data, with mixed results so far. In this first task-based functional magnetic resonance Imaging (fMRI) study of a normal individual with HSAM, dates were presented as cues and two phases were assessed during memory retrieval, initial access and later elaboration. Results showed that initial access was very fast, did not activate the hippocampus, and involved activation of predominantly posterior visual areas, including the precuneus. These areas typically become active during later stages of elaboration of personal memories rather than during initial access. Elaboration involved a balanced bilateral activation of most of the autobiographical network areas, rather than the more typical shifts observed in people without HSAM. Overall, the pattern of brain activations, which rests on repeated observations in a single individual, highlights a strong involvement of the precuneus and an idiosyncratic initial access to personal memory representations. Implications for the nature of personal memories in HSAM are discussed.

Introduction

Memory for personal events is typically far from perfect. Although people can remember personal events across their lifespan, with a clear increase for young adulthood experiences (reminiscence bump, e.g. Jansari & Parkin, 1996), usually only a handful of events are remembered in detail for each year of life. Two recent single-case reports (Ally et al., 2013, Parker et al., 2006), and four group studies (LePort et al., 2012, LePort et al., 2016, LePort et al., 2017, Santangelo et al., 2018) however, have challenged the limits of autobiographical memory. The case studies (Ally et al., 2013, Parker et al., 2006) described two individuals with the exceptional ability to remember in detail almost every day of their life (Ally et al., 2013, Parker et al., 2006). This rare ability, which has been called either hyperthymesia (Parker et al., 2006) or highly superior autobiographical memory (HSAM), questions the current thinking about autobiographical memory (hereinafter autobiographical memory (ABM)) as being of limited capacity.

The processes responsible for HSAM are still largely unknown, as unknown is whether ABM encoding and retrieval processes in these individuals function in a way similar to the normal population. Data on brain activation can provide valuable information on this issue as the network of areas involved in autobiographical memory in the normal population is relatively well known (e.g., Burianova et al., 2010, McGuire, 2001, Svoboda et al., 2006). Activation data in individuals with HSAM can reveal the extent to which the same network of brain areas is involved as found in the normal population or whether new areas, typically not part of the autobiographical memory network are also involved. In the present study we examine the brain activation of a new case of HSAM who, differently from the two previously published cases, and the individuals examined in LePort et al., 2016, LePort et al., 2017 and Santangelo et al. (2018) has no form of pathology. The case described by Ally et al. (2013) was an individual who was completely blind from birth, a condition that might have changed encoding processes, and determined the reorganization of a number of brain areas, including those involved in personal memories. Indeed, it is difficult to know which differences in brain structure may be due to blindness and which may be accountable by superior memory. The neuropsychological battery used by Parker et al. (2006) in the first reported case revealed the presence of a dysexecutive syndrome, accompanied by a form of Obsessive Compulsive Disorder (OCD). In addition, the woman described by Parker et al. (2006) kept a very detailed diary of her entire life, that she constantly rehearsed, which by some has been considered the factor responsible for her exceptional memory (e.g. Marcus, 2009). Consequently, these two case reports offer only limited insight into this exceptional condition.

A study reporting structural brain data on a group of 11 individuals with HSAM (LePort et al., 2012) used four brain imaging methods to compare brain structure in HSAM and controls. Local concentration of grey and white matter in any given voxel throughout the brain was assessed with Voxel Based Morphometry Grey-Matter (VBM-GM) and Voxel Based Morphometry WhiteMatter (VBM-WM); Diffusion Tensor Imaging-Fractional Anisotropy (DTI-FA) assessed differences with controls in white-matter microstructure, while differences in shapes of brain regions were examined using Tensor Based Morphometry (TBM). Results identified nine brain regions that, depending on the type of neuroanatomical analysis used, discriminated HSAM from control in terms of concentration of grey/white matter, shape of the region and white matter tract coherence. These regions include the inferior and middle temporal gyri and temporal pole (BA 20, 21 and 38, respectively), the anterior insula, the parahippocampal gyrus, (BA 36) and the inferior parietal sulcus. White matter tract coherence was also higher in HSAM participants. While these data provide additional insight into potential differences between individuals with HSAM and controls, attributing functional differences to structural differences can be somewhat problematic. As the authors themselves recognize “It is not known of course, whether the anatomical differences observed in our analyses are enabling or resulting from HSAM participants' memory performance.” (p. 16). They also recognize that some of these anatomical differences might not be linked to HSAM per se, rather to OCD, that was observed in more than half of the participants.

Very recently, a study (Santangelo et al., 2018) reported functional magnetic resonance imaging (fMRI) data on a group of individuals with HSAM and a control group. Participants were presented with cues that referred to the first or the last time a specific event happened, for example “The last time you took a train” or “The first train ride”. While memory performance was good among their HSAM participants, their results might be linked to the specific characteristics of the retrieval processes triggered by this type of material. These verbal cues not only refer to specific events in a person's life, they already contain elements of it. These results provide important information on brain areas activated in HSAM individuals while trying to remember these ‘first time’ and ‘last time’ specific events. However, what HSAM is characterized by is extensive retrieval of personal memories in response to dates. Five more HSAM individuals tested in our lab, but not reported here, while being superior to the control group also in response to event cues, truly excelled only when responding to dates.

We aimed at addressing some of the concerns and gaps of previous studies by examining in a single-case study a 21 year-old adult, BB, who presented no sign of OCD, autism, or other pathological conditions, who had no physical impairment, and had a normal-to-high level of intelligence. In response to dates, BB was able to remember almost every day of his life from approximately age 11. The detailed study of this case, which includes fMRI data, in addition to describing the specific characteristics of this individual, might contribute novel insight into the processes responsible for HSAM. His functional brain activation was assessed against previous group data examining areas that are active in the Autobiographical Memory Network.

Autobiographical memory is in itself a highly complex system involving a large number of cognitive and non-cognitive components. Cognitive components include episodic and semantic processing (Conway & Pleydell-Pearce, 2000), executive functions (Cabeza & Nyberg, 2000), mental imagery (Ogden, 1993), emotion (Addis, Moscovitch, Crawley, & McAndrews, 2004) and self-referential processes (e.g. D'Argembeau et al., 2010, Gusnard et al., 2001, Craik et al., 1999).

Major reviews of brain imaging studies of ABM (e.g. Maguire et al., 2001, Svoboda et al., 2006) have revealed a core network of areas involved in remembering one's personal past. These areas include cortical and subcortical regions in both hemispheres. Maguire (2001), in a review of the first 11 neuroimaging (positron emission tomography (PET) and fMRI) studies of retrieval from ABM, identified a network of predominantly left lateralized cortical areas which included retrosplenial/posterior cingulate cortex, medial temporal regions, the temporoparietal junction, medial prefrontal cortex (Brodmann areas 10,11,9), temporopolar cortex and cerebellum. A more recent meta-analysis of 24 functional studies of ABM retrieval by Svoboda et al. (2006) supported Maguire's (2001) earlier findings. These authors also proposed a distinction between a core network of structures activated across most ABM imaging studies (at least in 10 of the 24 studies examined) and two other sets of structures that are less present (secondary regions) or only rarely present (tertiary regions) in the 24 studies. The core network included the medial and lateral temporal cortex, the temporoparietal junction, the medial and lateral retrosplenial/posterior cingulate cortex, the cerebellum, and the ventrolateral prefrontal cortex. Compared to the pattern identified by Maguire et al., 2001, Svoboda et al., 2006 observed less involvement of the temporopolar cortex, and a more prominent role for the ventrolateral prefrontal and lateral temporal cortices, which have been thus included by Svoboda et al. in the core network. The secondary regions (those activated in at least five of the studies) were areas in the dorsolateral prefrontal cortex (BA 9, 9/46, 46), superior medial and superior lateral cortex (BA 6), anterior cingulate (BA 25, 32, 24), medial orbitofrontal, temporopolar and occipital cortex, thalamus and amygdala. Tertiary regions, found in less than 5 studies, were the frontal eye fields, motor cortex, medial (precuneus) and lateral parietal cortex, fusiform gyrus, superior and inferior lateral temporal cortex, insula, basal ganglia and brainstem.

While the pattern described above is the typical pattern of brain activation associated with retrieval from ABM in normal individuals who can remember some but certainly not all their past experiences, still little is known, so far, about patterns of activation in individuals with HSAM. Assessing the extent to which areas activated during retrieval in our HSAM case match the core network of areas described by Svoboda et al. (2006) in their meta-analysis represents then an important step in understanding this condition.

In this study, functional magnetic resonance imaging (MRI) data were obtained using dates as cues and a novel event-related activation paradigm structured to capture essential differences in the time course of ABM retrieval. The method followed closely the procedure by Daselaar et al. (2008). Brain activity was modelled in two ways, firstly when the memory initially surfaced to mind (initial access), and secondly during elaboration, when the memory was fully formed and detailed. In the average individual, initial access can be relatively fast (<5 sec) in the rare cases of direct retrieval (see Conway & Pleydell-Pearce, 2000), while the process of retrieving a fully detailed autobiographical memory is a relatively lengthy reconstructive process (e.g. Conway, 2005), making it possible to map the time course of changes in brain activation, and differentiate areas contributing to the initial access to a memory from those involved in the subsequent elaboration. Examining brain activation both when memory is accessed and when it is elaborated provides an additional advantage for modelling, as the variability in the time to access a memory represents an inherent ‘‘jitter’’ between the time of the cue and access to the memory (Daselaar et al., 2008). While in the scanner, our participant was asked to indicate when a memory had first surfaced to mind in response to cues. In our case cues were individual dates (e.g. 17th July 2000), as the ability to respond with memories to dates is a specific marker of HSAM. When still in the scanner, our participant was also asked to indicate again when the memory was fully formed and detailed. Daselaar et al. (2008) found that initial access (i.e., early stage of retrieval) to individual memories recruited the right hippocampus as well as retrosplenial, medial and the right prefrontal cortex, whereas visual areas, including the precuneus, and left prefrontal cortex showed increase in activation at a later time, during elaboration of individual memories when more details were added (see also Cabeza & St Jacques, 2007). Ours is the first study of task-based brain activation in a single HSAM individual with no sign of OCD, and as such it has mainly an exploratory aim, with the potential to show that OCD is not a necessary trait in determining HSAM.

Section snippets

Participants

Our HSAM participant, BB, was a healthy male, aged 20 at the time of testing. He was a second-year undergraduate student at a UK University. Informed consent was obtained before starting the study. On some cognitive and neuropsychological tasks, we also tested a control group of 17 individuals of the same age and education level of BB (age range 20–21, 9 females). A control group of 10 adults of the same age and education level was tested in the scanner to obtain structural data. The study was

Behavioural results

Autobiographical memory tests. Clear evidence of BB's exceptional ability to remember personal events was found in the tests which examined personal memories triggered by dates. BB was able to report at least one detailed memory for 88.4% of the dates presented. The control group reported an average of .03% memories for the dates presented. In the few instances in which controls could retrieve a memory in response to dates, retrieval time was 11.52 sec. In BB, consistency analysis showed that

Discussion

The behavioural data obtained in BB confirm that his is a clear case of HSAM, with no form of cognitive impairment and the ability to retrieve almost every day of his life starting from age 11. His performance on the various autobiographical memory tasks was extremely high, with a fast retrieval and high levels of test–retest consistency in his personal memory reports (which indicates that these were not made-up confabulations). Personal memories were mainly reported as being visual. BB

Conclusions

The results of the functional brain imaging procedure in BB reveal an overall pattern that seems to be rather specific to this case, but might also be common to other individuals with HSAM. It is almost the opposite of that observed in individuals who don't possess an exceptional personal memory. A larger grey matter in posterior areas, as well as a predominantly posterior activation already during access reinforce the observation about the highly predominant role of visual areas during the

Compliance with ethical standards

None of the authors has a conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Pre-registration

No part of the study procedures and analyses was pre-registered prior to the research being conducted.

Funding

This work was in part supported by a University of Hull 80th Anniversary fund; Channel 4; The British Academy grant n. YHB085; all to the first author.

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