Memory

Memory
Our memory research has focused on naturalistic expressions of memory, particularly autobiographical memory, which refers to processing of information concerning events and facts from one's past. The distinction between episodic and semantic memory, originally delineated by professor Endel Tulving, has been influential in our research. Episodic autobiographical memory concerns recollection of specific events, accompanied by a state of consciousness that marks the experience as part of one's personal history. Semantic autobiographical memory concerns historical facts, traits, knowledge states that are not linked to a specific time and place (for review, see Renoult et al., 2012). Our research is focused on the functional and neuroanatomical substrates of these two types of mnemonic capacities. This research was instigated by patient M.L., who had isolated retrograde amnesia specific to episodic autobiographical memory following a severe brain injury (Levine et al., 1998, 1999; Levine et al., 2009).

Table of Contents
The Autobiographical Interview (AI) and assessment of autobiographical memory
- Table of studies using the Autobiographical Interview
The Air Transat Study
Individual differences in autobiographical memory
Severely Deficient Autobiographical Memory (SDAM)
Functional Neuroimaging

The Autobiographical Interview (AI) and assessment of autobiographical memory
The Autobiographical Interview (AI; Levine et al., 2002) is a method of assessing autobiographical memory from within a single narrative using a text-based analysis of transcribed autobiographical protocols. The AI provides a wealth of information concerning elements of naturalistic autobiographical memory. Most importantly, the scoring method separates episodic details (i.e., description of the event, sensory or mental state details specific to the event) from non-episodic details (i.e., semantic or factual statements, or other details not specific to the event). We refer to these as internal and external details.

The AI has been used in over 200 studies in healthy and patient samples (click here for a full list). It has proven useful to test theories concerning the nature of memory loss in patients with medial temporal lobe damage (Addis et al., 2007; Rosenbaum et al., 2008; St.-Laurent et al., 2009), including patient H.M. (Steinvorth et al., 2005). It has also been used to characterize naturalistic mnemonic deficits in mild cognitive impairment (MCI; Murphy et al., 2008), Alzheimer’s disease (Irish et al., 2011), traumatic brain injury (Esopenko & Levine, 2017) depression (Söderlund et al., 2014), and frontotemporal lobar degeneration (FTLD; McKinnon et al., 2006, 2008). Other studies have adapted the AI for assessment of autobiographical memory in typical and atypical development (Willoughby et al., 2012; Gascoigne et al., 2013) and in thinking about the future (Addis, Wong, & Schacter, 2008). Numerous studies have demonstrated a relationship between internal (episodic) details as measured by the AI and structural and functional measures of the medial temporal lobes (in addition to patient studies noted above, see for e.g., Hodgetts et al., 2017; Memel et al., 2020; Palombo et al., 2018).

The Air Transat Study
In 2001, Air Transat flight 236 ran out of fuel over the Atlantic Ocean. After 30 terrifying minutes in which the passengers and crew prepared to ditch into the ocean, the pilot miraculously glided the jet to an Azores airbase with no injuries. Our team, including Margaret McKinnon , Daniela Palombo , Rebecca Todd , and Adam Anderson, have been studying the effects of this trauma on memory and attention. Using the Autobiographical Interview, we showed that memory for details of the Air Transat disaster was greatly enhanced, but this enhanced vividness was not associated with the presence of post-traumatic stress disorder (PTSD; McKinnon, Palombo et al., 2015). On the other hand, those with PTSD generated an excess of external details. This effect was observed for all events tested, not just the Air Transat disaster, suggesting that strategic control over memory may be altered in those who develop PTSD. These findings may be useful in understanding why some develop PTSD while others do not, even when exposed to the same traumatic event.

We next probed the neural correlates of traumatic memory enhancement in a subset of passengers scanned with fMRI 9 years after the Air Transat disaster (Palombo et al., 2016). Passengers were scanned while viewing video recreations of the event from NBC and the Discovery Channel as part of the media coverage at the time of the event, along with footage of the events of September 11, 2001 and a neutral event. After the scans, passengers' narrative descriptions of the events were scored using the Autobiographical Interview. As in our prior study, passengers showed a strong memory enhancement effect for the traumatic event. The degree of memory enhancement was correlated with activation in the bilateral amygalae, along with medial temporal regions, the ventral visual system, and anterior and posterior midline regions. The same pattern was observed in relation to memory for September 11, 2001. This is the first fMRI study of memory for a life-threatening event in a group of individuals with homogenous traumatic exposure. The correspondence of traumatic memory enhancement with amygdalar activation supports the role of this structure in memory for remotely occurring trauma, and further suggests mechanisms for memory vividness of both traumatic and non-traumatic events.

Behavioral PLS analysis results showing correspondence of memory vividness (internal details from the Autobiographical Interview) for the AT disaster and September 11, 2001 with amygdalar activation.

Individual differences in autobiographical memory

Some remember events vividly while others have only a vague recollection of the same events. Similarly, some efficiently access factual information, such as news events or trivia, whereas others do not. To our knowledge, such individual differences in naturalistic memory have not been investigated, although there have been studies concerning individual differences in performance on laboratory tasks. We believe that "trait mnemonics" reflect potentially valid individual difference characteristics, much like personality traits, that may have implications for cognitive function (for review, see Palombo et al, 2018). We developed the Survey of Autobiographical Memory (SAM; Palombo et al., 2013), a questionnaire designed to assess individual differences in episodic, semantic, and spatial memory, as well as future thinking. In a web-based study of 600 volunteers, this test was validated in relation to laboratory measures as well as sex differences and the effects of depression.

Episodic autobiographical memory related to posterior MTL connectivity (warm colors), semantic ability related to anterior MTL connectivity (cool colors)

Sheldon et al (2016) recently demonstrated that individual differences in trait mnemonics as measured by the SAM are related to intrinsic functional connectivity as measured by resting state functional MRI (i.e., brain activity in the absence of overt task demands). Endorsement of strongly vivid episodic memory was associated with increased connectivity between the medial temporal lobes and posterior regions. That is, individuals who report high episodic autobiographical memory in their day-to-day lives show increased connectivity in memory networks involved in accessing images and other perceptual information. Endorsement of high factual or semantic memory showed a different pattern: enhanced connectivity between the medial temporal lobes and prefrontal regions involved in organization and integrating conceptual information. These findings suggest that individual differences in how people remember the past correspond to functional brain organization at rest. We are currently investigating the relationship of memory traits on the SAM to other tests of memory and personality as well as targeted genetic polymorphisms.

One way to study memory abilities is to manipulate or interfere with them in an experiment. Sheldon et al (2016) tested memory for video stimuli while participants were watching a screen with Dynamic Visual Noise (DVN) or a solid grey screen. DVN interferes with the ability to form images. We also asked participants to rate their visual imagery abilities on a questionnaire. Individual differences in visual imagery abilities interacted with DVN such that the higher ones visual imagery ratings, the greater the effect of DVN. In other words, individuals who readily form visual images showed greater interference effects during DVN, whereas those who with lower visual imagery abilities were less affected by this manipulation. This study reinforces a link between visual imagery and memory.

DVN interference effect is correlated with spatial imagery abilities

Severely Deficient Autobiographical Memory (SDAM)
SDAM refers to a lifelong inability to vividly relive or re-experience personal events. Palombo, Alain and colleagues (2015) report data from three healthy, high functioning individuals with SDAM and matched controls intensively studied in our laboratory. We found that these individuals had reduced visual memory on laboratory tasks, reduced right hippocampal volume, and reduced activation of the canonical autobiographical memory network during fMRI scanning. They also showed a greatly reduced late positivity Event Related Potential (ERP) component of recognition memory for pictures presented in a laboratory experiment, in spite of the fact that their recognition memory performance was intact. The late positivity ERP component indicates conscious recollection or re-experiencing of the test item. This latter finding suggests that intact memory performance (and day-to-day memory function) in SDAM is may be supported by non-episodic processes (e.g., semantic memory, familiarity). We are currently investigating the behavioural and neural correlates of SDAM and individual differences more generally. More information about SDAM can be found here. To participate in our online memory survey, click here.

Functional neuroimaging
Functional imaging techniques enable the examination of the neuroanatomical correlates of memory in healthy adults, complementing our behavioural research in aging and clinical samples. Data from functional neuroimaging studies of autobiographical memory have documented a network of regions supporting autobiographical memory that is distinct from networks supporting performance on laboratory tasks, but overlapping with the brain's default mode network that is associated with self-related cognition (Svoboda, McKinnon, and Levine, 2006).

We have sought to increase the fidelity of autobiographical stimulation by using a prospective "diary" method whereby research participants are scanned during replay of audio recordings that they made contemporaneously with events from their own past. This method allows for a high degree of control over autobiographical stimuli that cannot be attained with retrospective methods that are typically used in functional neuroimaging studies of autobiographical memory. Using this method, we have demonstrated distinct networks associated with vivid recall of verified episodic and semantic autobiographical information (Levine et al., 2004) and the effects of memory characteristics including rehearsal and age of autobiographical events on medial temporal lobe activation (Svoboda et al., 2009; Sheldon & Levine, 2013; also see Söderlund et al., 2012).

Magnetoencephalography (MEG) data using this paradigm have been used to show how coupling or synchrony of theta oscillations in medial temporal and anteromedial prefrontal regions support subjective vividness in autobiographical recall (Fuentemilla et al., 2014) and how information-theoretic measures dissociate episodic and semantic autobiographical recall (Heisz et al., 2013). In line of research led by Louis Renoult, the neural correlates of different elements of personal semantic memory (e.g. autobiographically significant factual knowledge vs. general semantic knowledge) have been dissociated using event related potentials (ERPs; Renoult et al., 2014).