The Role of Relational Binding in Item Memory: Evidence from Face Recognition in a Case of Developmental Amnesia

Abstract

Current theories state that the hippocampus is responsible for the formation of memory representations regarding relations, whereas extrahippocampal cortical regions support representations for single items. However, findings of impaired item memory in hippocampal amnesics suggest a more nuanced role for the hippocampus in item memory. The hippocampus may be necessary when the item elements need to be bound within and across episodes to form a lasting representation that can be used flexibly. The current investigation was designed to test this hypothesis in face recognition. H.C., an individual who developed with a compromised hippocampal system, and control participants incidentally studied individual faces that either varied in presentation viewpoint across study repetitions or remained in a fixed viewpoint across the study repetitions. Eye movements were recorded during encoding and participants then completed a surprise recognition memory test. H.C. demonstrated altered face viewing during encoding. Although the overall number of fixations made by H.C. was not significantly different from that of controls, the distribution of her viewing was primarily directed to the eye region. Critically, H.C. was significantly impaired in her ability to subsequently recognize faces studied from variable viewpoints, but demonstrated spared performance in recognizing faces she encoded from a fixed viewpoint, implicating a relationship between eye movement behavior in the service of a hippocampal binding function. These findings suggest that a compromised hippocampal system disrupts the ability to bind item features within and across study repetitions, ultimately disrupting recognition when it requires access to flexible relational representations.

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

“…Lesions in each of the PRC, ERC, and PHC resulted in slower signal from the hippocampus throughout the network and, ultimately, to oculomotor regions. Relatively faster signal from MTL regions could result in an increase in visual exploration behavior, consistent with a case study of amnesia . Information regarding the relations among items, the broader environment, and/or the spatial organization of intra‐ or inter‐item features, as supported by the hippocampus, PHC, and ERC, respectively, may be slow to develop and/or ineffective in the guidance of gaze fixations .…”

“…In fact, the very way in which information is viewed may be fundamentally altered with hippocampal compromise, even when there is no memory task at hand. Whereas neurologically intact adults tended to explore all the features of a face during viewing, a developmental amnesic case with congenital abnormalities to the hippocampus, fornix, and mamillary bodies showed an increased amount of visual sampling and a viewing pattern that was predominantly focused on a single face feature . In the face of compromised hippocampal function, representations of sampled information are not developed over time and do not affect ongoing viewing behavior, leading to altered viewing patterns compared with neurologically intact viewers.…”

Modelling the influence of the hippocampal memory system on the oculomotor system

“…Eyetracking has been used as a tool to probe the integrity of function in the hippocampus (HC) and regions of the broader medial temporal lobe (MTL), which are critical for the formation and use of memory representations (see Hannula et al, 2010, for review). Amnesic cases who have compromised HC and/or MTL show specific changes in their viewing behavior compared to healthy individuals (Ryan et al, 2000;Warren et al, 2010;Olsen et al, 2015). Similar findings have been observed in older adults who have suspected HC/MTL compromise , and certain viewing patterns have been shown to track with entorhinal cortex (ERC) volumes (Yeung et al, 2017).…”

“…Complementary neuroimaging evidence in humans has shown that visual sampling (number of gaze fixations) is predictive of HC activity (Liu et al, 2017). In macaques and humans, damage to the HC/MTL results in altered visual exploration (Chau et al, 2011;Olsen et al, 2015) and HC responses in humans are predictive of subsequent gaze patterns that express memory retrieval (Hannula & Ranganath, 2009;Ryals et al, 2015). Such evidence collectively demonstrates that neural integrity and/or function within the HC/MTL is related to oculomotor behavior.…”

Focus group reflections on the current and future state of cognitive assessment tools in geriatric health care

“…In healthy adults, eye movement patterns of memory correlate with medial temporal lobe activity 7. Amnesic patients, who have severe memory deficits due to lesions in the medial temporal lobes, do not show the same eye movement patterns as people who have normal memory function 8–11. More recent work has shown that by using machine-learning techniques, measures derived from eye-tracking may be used to accurately detect cognitive deficits in individuals with MCI 12.…”