Item familiarity and controlled associative retrieval in Alzheimer's disease: An fMRI study

Abstract

Typical Alzheimer's disease (AD) is characterized by an impaired form of associative memory, recollection, that includes the controlled retrieval of associations. In contrast, familiarity-based memory for individual items may sometimes be preserved in the early stages of the disease. This is the first study that directly examines whole brain regional activity during one core aspect of the recollection function: associative controlled episodic retrieval (CER), contrasted to item familiarity in AD patients. Cerebral activity related to associative CER and item familiarity in AD patients and healthy controls (HC) was measured with functional magnetic resonance imaging during a word-pair recognition task to which the process dissociation procedure was applied. Some patients had null CER estimates (AD-), whereas others did show some CER abilities (AD+), although significantly less than HC. In contrast, familiarity estimates were equivalent in the three groups. In AD+, as in controls, associative CER activated the inferior precuneus/posterior cingulate cortex (PCC). When performing group comparisons, no region was found to be significantly more activated during CER in HC than AD+ and vice versa. However, during associative CER, functional connectivity between this region and the hippocampus, the inferior parietal and dorsolateral prefrontal cortex (DLPFC) was significantly higher in HC than in AD+. In all three groups, item familiarity was related to activation along the intraparietal sulcus (IPS). In conclusion, whereas the preserved automatic detection of an old item (without retrieval of accurate word association) is related to parietal activation centred on the IPS, the inferior precuneus/PCC supports associative CER ability in AD patients, as in HC. However, AD patients have deficient functional connectivity during associative CER, suggesting that the residual recollection function in these patients might be impoverished by the lack of some recollection-related aspects such as autonoetic quality, episodic details and verification.

Cognitive and neuroimaging evidence of impaired interaction between self and memory in Alzheimer's disease

“…In a previous fMRI study of memory retrieval in HC participants and AD patients, we found that despite lower recollection-based performance than HC participants, AD patients activated the PCC as HC participants. Connectivity analyses in this previous study revealed, however, that functional connectivity of the PCC during episodic retrieval was impaired in AD patients (Genon, Collette, Feyers et al, 2013). This suggests that brain functioning supporting recollection-related processes is complex and that impaired recollection function in AD patients might be related to subtle functional changes (probably in terms of connectivity) within a large-scale brain network.…”

“…Alzheimer's disease (AD) is characterized by impaired recollection-based processes, such as controlled retrieval (Knight, 1998;Smith and Knight, 2002;Adam et al, 2005;Genon, Collette, Feyers et al, 2013) and experience of remembering (Dalla Barba, 1997;Rauchs et al, 2007). In the same line, the quality of the recollective experience for autobiographical memories is impaired in AD patients (Irish, Hornberger, et al, 2011;Irish, Lawlor, et al, 2011;Piolino et al, 2003).…”

“…The authors found that retrieval of items that had been encoded in reference to the self was related to brain activation in the posterior cingulate cortex (PCC) in healthy young adults (Leshikar & Duarte, 2012). The PCC has been found to play a role in both episodic retrieval (Genon, Collette, Feyers et al, 2013) and self-related processes (D'Argembeau et al, 2008; for a review see Andrews-Hanna, 2012). Therefore, the PCC could potentially play a role in the retrieval of self-related information in episodic memory.…”

Relating pessimistic memory predictions to Alzheimer's disease brain structure

“…In a previous study (Genon et al, 2013), we found that AD patients showed activation of the PCC (which is assumed to be a crucial cortical hub in higher cognitive processes such as episodic memory retrieval (Leech and Sharp, 2014)) during episodic retrieval as healthy older participants did, while they showed 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 impaired functional connectivity between PCC on the one hand and hippocampus and lateral prefrontal cortex (LPFC) on the other hand. This suggested that impaired controlled/conscious retrieval of recent episodic memories in AD patients might be related to disconnection within a wide brain network.…”

“…One striking feature highlighted by previous fine examination of memory retrieval of recent memories in AD patients is the dissociation between automatic and controlled processes with the former being relatively preserved (based on familiarity or fluency for the memory trace) while controlled and conscious access to recently encountered information in memory (i.e. episodic memory retrieval) is particularly impaired (Dalla Barba, 1997;Genon et al, 2014;Genon et al, 2013). One relevant aspect that can be examined to better understand the neurocognitive mechanisms of episodic memory retrieval in AD is the insight or subjective judgment that the patients have on their current memory functioning when they are in the context of retrieving information from memory.…”