Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition

Abstract

Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.

When memory does not fail: Familiarity-based recognition in mild cognitive impairment and Alzheimer's disease.

“…Hypoxic patients showed intact familiarity, whereas patients with more extensive medial temporal damage showed impaired familiarity, consonant with the view that the contribution of the hippocampus to familiarity is minimal. Additional evidence likewise indicates that patients with damage restricted to the hippocampus can show relatively preserved familiarity with impaired recollection (Aggleton et al, 2005;Baddeley, Vargha-Khadem, & Mishkin, 2001;Bastin et al, 2004;Holdstock et al, 2002;Mayes et al, 2004). Studies that have assessed recognition in patients with extensive medial temporal damage have found that these patients generally exhibited recognition deficits in both recollection and familiarity (Giovanello & Verfaellie, 2001;Knowlton & Squire, 1995).…”

Course of relational and non-relational recognition memory across the adult lifespan

“…Evidence for the dissociability of relational and item/non-relational recognition stems from fMRI studies of differential hippocampus vs. perirhinal cortex/anterior parahippocampal cortex activations associated with the two types of memory (Pihlajamaki et al 2004;Kohler et al 2005;Daselaar et al 2006;Montaldi et al 2006). Studies of patients with hippocampal lesions have as yet not yielded a clear picture with respect to the dissociability of relational and non-relational memory Manns et al 2003;Mayes et al 2004;Wixted and Squire 2004;Wais et al 2006;Wixted 2007). Interestingly, single-unit recordings in human epilepsy patients demonstrated that hippocampal neurons show a familiarity response in the absence of successful recollection, but notably also in the absence of successful non-relational recognition (Rutishauser et al 2006).…”

“…The perirhinal cortex was shown to be involved in the perceptual analysis of single items and in binding of individual stimulus features into a coherent representation of an object, which requires perceptual and mnemonic competence (Bussey et al 2002;Buckley 2005;Bussey and Saksida 2005). It may support relational processing under some circumstances, such as unitizing two features of the same kind to one single item or merged unity representation, but not spatiotemporal relational associations (Norman and O'Reilly 2003;Mayes et al 2004;Jager et al 2006). The hippocampus, on the other hand, mediates associations of the same kind such as object-object associations (Kesner and Hopkins 2006).…”

Hippocampal Complex Contribution to Retention and Retrieval of Recent and Remote Episodic and Semantic Memories: Evidence from Behavioral and Neuroimaging Studies of Healthy and Brain-Damaged People

“…Damage to this system causes deficits in spatial memory and in memory for complex relational information that typifies memory for autobiographical episodes, but spares recognition based only on familiarity (Aggleton et al, 2000;Holdstock et al, 2002a;Mayes et al, 2002Mayes et al, , 2004D. Moscovitch & McAndrews, 2002;Yonelinas, 2002;Yonelinas et al, 2002).…”

“…A number of studies showed that recollection was disproportionately impaired following lesions that included the hippocampus, whereas familiarity was relatively spared (Holdstock et al, 2002a, b;Mayes et al, 2003Mayes et al, , 2004D. Moscovitch & McAndrews, 2000;Yonelinas et al, 2002).…”