Impaired recollection but spared familiarity in patients with extended hippocampal system damage revealed by 3 convergent methods

Vann, Seralynne Denise; Tsivilis, Dimitris; Denby, Christine; Quamme, Joel R.; Yonelinas, Andrew P.; Aggleton, John Patrick; Montaldi, Daniela; Mayes, Andrew R.

doi:10.1073/pnas.0812097106

Cited by 172 publications

(167 citation statements)

References 31 publications

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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%

“…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).…”

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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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Section: Discussionmentioning

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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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“…As focal damage to the fornix and mammillary bodies results in impaired performance that resembles that of hippocampal damage (Dusoir et al 1990;Tsivilis et al 2008;Rudebeck et al 2009;Vann et al 2009b), it has been suggested the study of hippocampusbased memory should be extended to include the fornix and mammillary bodies as part of the "extended hippocampal system" (Aggleton and Brown 1999).…”

Section: Hippocampus and Mtlmentioning

confidence: 99%

Memory Retrieval in Mice and Men

Ben-Yakov

Dudai

Mayford

2015

Cold Spring Harb Perspect Biol

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Retrieval, the use of learned information, was until recently mostly terra incognita in the neurobiology of memory, owing to shortage of research methods with the spatiotemporal resolution required to identify and dissect fast reactivation or reconstruction of complex memories in the mammalian brain. The development of novel paradigms, model systems, and new tools in molecular genetics, electrophysiology, optogenetics, in situ microscopy, and functional imaging, have contributed markedly in recent years to our ability to investigate brain mechanisms of retrieval. We review selected developments in the study of explicit retrieval in the rodent and human brain. The picture that emerges is that retrieval involves coordinated fast interplay of sparse and distributed corticohippocampal and neocortical networks that may permit permutational binding of representational elements to yield specific representations. These representations are driven largely by the activity patterns shaped during encoding, but are malleable, subject to the influence of time and interaction of the existing memory with novel information.

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“…5 To assess episodic memory in more detail in MCI, it was important to select measures that minimized the risk of patients performing at floor level. The visual recognition test from the Doors and People Test 23 and the face recognition test from the Camden Recognition Memory Test (CRMT) 24 have proven utility in amnestic patients 25 and were therefore chosen. Recollection-vs familiarity-based recognition processes were probed further in the CRMT with the "rememberknow" procedure.…”

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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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Impaired recollection but spared familiarity in patients with extended hippocampal system damage revealed by 3 convergent methods

Cited by 172 publications

References 31 publications

Extent of hippocampal atrophy predicts degree of deficit in recall

Extent of hippocampal atrophy predicts degree of deficit in recall

Memory Retrieval in Mice and Men

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

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