Frontotemporal Connections in Episodic Memory and Aging: A Diffusion MRI Tractography Study

Metzler‐Baddeley, Claudia; Jones, Derek K.; Belaroussi, Boubakeur; Aggleton, John Patrick; O’Sullivan, Michael

doi:10.1523/jneurosci.2317-11.2011

Cited by 215 publications

(279 citation statements)

References 76 publications

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“…Although important for memory performance, we could not assess the fornix in our study because it is not part of the automated atlas we used and it is difficult to delineate this structure when using the tract-based spatial statistics approach. Furthermore, the different sensitivities of the FA and MD parameters led to few overlaps between the FA and MD findings, which has been described in previous neuroimaging studies 7 and did not impact on the interpretation of the results.…”

Section: Discussionsupporting

confidence: 61%

“…Previous studies have shown that memory function was associated with white matter integrity in the inferior and superior longitudinal fasciculi, the posterior and anterior cingulum 4 the uncinate fasciculus, the dorsal cingulum bundle 5 and the hippocampal part of the cingulum 6 . However, these studies have explored the correlation between episodic memory and white matter integrity in highly-educated individuals, selected under strict criteria from research centers 5,7 . Hence, the role of white matter integrity on episodic memory in community-dwelling elderly with a low educational level remains to be explored.…”

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confidence: 99%

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Integrity of white matter structure is related to episodic memory performance in the low-educated elderly

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Tovar‐Moll

Ferreira

et al. 2017

Arq. Neuro-Psiquiatr.

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Memory decline occurs in normal aging and is also a core feature of the most common cause of dementia, Alzheimer's disease 1 . As the prevalence of this disorder and other forms of dementia is higher in developing countries 2 , it is important to explore the neural correlates of episodic memory in the setting of low education, a situation extremely common among the elderly population in low-and middle-income countries. Hence, understanding the anatomic substrate of memory performance, especially in vulnerable individuals, can help to develop strategies to prevent cognitive decline in this scenario.Apart from the hippocampus and the medial temporal lobe structures, well-established episodic memory cortical correlates ABSTRACTThe low-educated elderly are a vulnerable population in whom studying the role of white matter integrity on memory may provide insights for understanding how memory declines with aging and disease. Methods: Thirty-one participants (22 women), 23 cognitively healthy and eight with cognitive impairment-no dementia, aged 80.4 ± 3.8 years, with 2.2 ± 1.9 years of education, underwent an MRI scan with diffusion tensor imaging (DTI) acquisition. We verified if there were correlations between the performance on the Brief Cognitive Screening Battery (BCSB) and the Rey Auditory Verbal Learning Test (RAVLT) with DTI parameters. Results: The BCSB delayed recall task correlated with frontotemporoparietal connection bundles, with the hippocampal part of the cingulum bilaterally and with the right superior longitudinal fasciculus. The RAVLT learning and delayed recall scores also correlated with the hippocampal part of the cingulum bilaterally. Conclusions: Although preliminary, our study suggests that the integrity of white matter frontotemporoparietal fasciculi seems to play a role in episodic memory performance in the low-educated elderly. This finding opens opportunities to study potential targets for memory decline prevention in vulnerable populations.Keywords: episodic memory; aging; white matter; health vulnerability. RESUMOIdosos de baixo nível educacional representam uma população vulnerável em que o estudo do papel da integridade da substância branca na memória pode revelar como essa declina no envelhecimento. Métodos: Trinta e um indivíduos (22 mulheres), sendo 23 cognitivamente saudáveis, oito com comprometimento cognitivo não demência, 80,4 ± 3,8 anos de idade e 2,2 ± 1,9 anos de escolaridade, foram submetidos à RM com imagem de tensor de difusão, cujos parâmetros foram correlacionados com a Bateria Cognitiva Breve (BCSB) e o Teste Auditivo Verbal de Rey (RAVLT). Resultados: A evocação tardia da BCSB correlacionou-se com fascículos de conexão frontotemporoparietal, fascículo longitudinal superior direito e cíngulo parte hipocampal bilateral, sendo que esse último também correlacionou com o RAVLT (aprendizado e evocação tardia). Conclusão: Apesar de preliminar, nosso estudo sugere que a integridade da substância branca parece ser importante para a memória em idosos de baixa escolaridade, achad...

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Section: Discussionsupporting

confidence: 61%

mentioning

confidence: 99%

Integrity of white matter structure is related to episodic memory performance in the low-educated elderly

Resende

Tovar‐Moll

Ferreira

et al. 2017

Arq. Neuro-Psiquiatr.

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“…Previous reports using the D&P test had already indicated a selective effect of hippocampal damage on recall (7)(8)(9)(19)(20)(21)(22), but those studies did not examine whether this selective mnemonic effect was correlated with extent of hippocampal damage. Because our patient cohort was a large one and had wide variation in extent of hippocampal atrophy, we were able to examine this structure/function relationship and found a sharp distinction between recall and recognition performance, with only the former showing a correlation with extent of HV loss.…”

Section: Discussionmentioning

confidence: 99%

Extent of hippocampal atrophy predicts degree of deficit in recall

Patai

Gadian

Cooper

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Which specific memory functions are dependent on the hippocampus is still debated. The availability of a large cohort of patients who had sustained relatively selective hippocampal damage early in life enabled us to determine which type of mnemonic deficit showed a correlation with extent of hippocampal injury. We assessed our patient cohort on a test that provides measures of recognition and recall that are equated for difficulty and found that the patients' performance on the recall tests correlated significantly with their hippocampal volumes, whereas their performance on the equally difficult recognition tests did not and, indeed, was largely unaffected regardless of extent of hippocampal atrophy. The results provide new evidence in favor of the view that the hippocampus is essential for recall but not for recognition.long-standing issue in memory research is the identity of the mnemonic process served by each of the components of the medial temporal lobe (MTL). Recall, which is the ability to retrieve from memory a stimulus or its context that is no longer present, is a more complex function than recognition, which is the ability to identify a current stimulus as old or new, or to choose a previously encountered stimulus among competing distractors. Over the years, a large number of studies have been conducted, aiming to tease apart the relative contribution of different MTL structures to recall and recognition. Many investigators have proposed that these two distinct memory processes rely on different MTL structures, with recall being dependent on the hippocampus and recognition being supported by parahippocampal structures, such as the perirhinal and entorhinal cortices (1-5, but see ref. 6). Also, studies examining the effects of damage to the mammillary bodies and fornices, structures within the hippocampal circuit, have shown that volume loss is correlated with deficits in recall but not in recognition (7,8).However, there is also evidence suggesting that both processes rely on the hippocampus (for a review, see ref. 6). Most of the literature on either side of this controversy is composed of studies with single cases or small sample sizes. Indeed, to date, none of the studies involving humans has been able to demonstrate a clear relationship between memory process and hippocampal volume (HV), possibly due to lack of variability in HV loss. Additionally, many of the contradictory findings could result from measures used to test recognition and recall not being equated for level of difficulty.Previous work from our group demonstrated that patients with developmental amnesia due to severe hippocampal pathology sustained early in life are seriously impaired in their ability to recall visual or verbal stimuli but are relatively unimpaired in recognizing them (9). By identifying a group of patients with varying extents of HV reduction, and applying a standardized measure of memory [the Doors and People test (D&P test) (10)] in which the recognition and recall subtests are matched for difficulty, we were abl...

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“…Fornix microstructure accounts for both age-related and age-independent variations in free recall. 5 Recent diffusion MRI studies have found that fornix microstructure is compromised in MCI and Alzheimer disease. 6,7 Early damage might lead to engagement of alternative interactions, 8 so that episodic memory becomes disproportionately associated with microstructure of tracts other than the fornix.…”

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confidence: 99%

Temporal association tracts and the breakdown of episodic memory in mild cognitive impairment

et al. 2012

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Objective: To examine the pattern of association between microstructure of temporal lobe connections and the breakdown of episodic memory that is a core feature of mild cognitive impairment (MCI).Methods: Twenty-five individuals with MCI and 20 matched controls underwent diffusion MRI and cognitive assessment. Three temporal pathways were reconstructed by tractography: fornix, parahippocampal cingulum (PHC), and uncinate fasciculus. Tissue volume fraction-a tract-specific measure of atrophy-and microstructural measures were derived for each tract. To test specificity of associations, a comparison tract (corticospinal tract) and control cognitive domains were also examined.Results: In MCI, tissue volume fraction was reduced in the fornix. Axial and radial diffusivity were increased in uncinate and PHC implying more subtle microstructural change. In controls, tissue volume fraction in the fornix was the predominant correlate of free recall. In contrast, in MCI, the strongest relationship was with left PHC. Microstructure of uncinate and PHC also correlated with recognition memory, and recognition confidence, in MCI.Conclusions: Episodic memory in MCI is related to the structure of multiple temporal association pathways. These associations are not confined to the fornix, as they are in healthy young and older adults. In MCI, because of a compromised fornix, alternative pathways may contribute disproportionally to episodic memory performance. Breakdown of episodic memory is a core feature of mild cognitive impairment (MCI).1 Previous studies of MCI have focused on changes in the medial temporal lobe (MTL). However, the MTL is one node of wider networks for memory that include frontal and parietal lobes.2 The "extended hippocampal system" 3 incorporates the fornix-a large fiber tract composed mostly of connections associated with the hippocampal formation. 4 Alternatively, MTL-cortical interactions can be mediated by parahippocampal tracts including the uncinate fasciculus and the temporal portion of the cingulum bundle (parahippocampal cingulum [PHC]).In healthy older adults, the microstructure of the fornix is an established correlate of episodic memory performance. Fornix microstructure accounts for both age-related and age-independent variations in free recall.5 Recent diffusion MRI studies have found that fornix microstructure is compromised in MCI and Alzheimer disease. 6,7 Early damage might lead to engagement of alternative interactions, 8 so that episodic memory becomes disproportionately associated with microstructure of tracts other than the fornix. To test this hypothesis, diffusion MRI tractography was used to reconstruct the fornix, PHC, and uncinate in MCI and controls. Intrinsic microstructure and subtle atrophy were quantified separately 9,10 dealing with an important confound in MCI and aging.

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Frontotemporal Connections in Episodic Memory and Aging: A Diffusion MRI Tractography Study

Cited by 215 publications

References 76 publications

Integrity of white matter structure is related to episodic memory performance in the low-educated elderly

Integrity of white matter structure is related to episodic memory performance in the low-educated elderly

Extent of hippocampal atrophy predicts degree of deficit in recall

Temporal association tracts and the breakdown of episodic memory in mild cognitive impairment

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