Experience-Dependent Eye Movements, Awareness, and Hippocampus-Dependent Memory

Abstract

We asked what kind of memory is operating when eye movements change as the result of experience. Participants viewed scenes that were either novel, repeated, or manipulated (i.e., a change was introduced in one region of the scene). Eye movements differed depending on the past viewing history of each scene. Participants made fewer fixations and sampled fewer regions when scenes were repeated than when scenes were novel. When scenes were altered, participants made more fixations in the altered region, spent more time looking at the altered region, and made more transitions into and out of the altered region than in unchanged (matched) regions in the repeated scenes. Importantly, these effects occurred only when individuals were aware that a change had occurred. Participants who were unaware that the scene had been altered looked at the changed scenes in the same way that they looked at repeated scenes. Thus, there was no indication that eye movements could reveal an unaware (unconscious) form of memory. Instead, eye movements reflected conscious memory of whether the scene was repeated or manipulated. The findings were the same when awareness was assessed after viewing all the scenes (experiment 1) and when awareness was assessed after each scene was presented (experiment 2). In experiment 3, memory-impaired patients with damage limited to the hippocampus were impaired at deciding whether scenes were novel, repeated, or manipulated. Thus, the ability to consciously recollect recent encounters with scenes reflects a form of hippocampus-dependent memory. The findings show that experience-dependent eye movements in response to altered scenes reflect conscious, declarative memory, and they support the link between aware memory, declarative memory, and hippocampus-dependent memory.

Unconscious Relational Inference Recruits the Hippocampus

“…The finding of a hippocampal involvement in unconscious relational integration and inference is at odds with classic notions of human long-term memory that segregate memory systems according to consciousness of encoding and retrieval (Tulving, 2002;Squire, 2004;Smith et al, 2006;Squire and Wixted, 2011).…”

Has someone moved my plate? The immediate and persistent effects of object location changes on gaze allocation during natural scene viewing

“…Ryan and Cohen, for example, examined the effect of spatial location changes on implicit and explicit change detection by subsequently presenting pairs of scenes in which objects were deleted, added, or moved. Gaze toward changed objects was increased even when these changes were not accessible for verbal report (see also Hayhoe, Bensinger, & Ballard, 1998;Henderson & Hollingworth, 2003;Hollingworth, Williams, & Henderson, 2001; but see Smith, Hopkins, & Squire, 2006). Although these findings support the view that changes to stored scene representations are able to exhibit control over eye movement behavior, it remains unclear how long these effects persist.…”

Hippocampal differentiation without recognition: An fMRI analysis of the contextual cueing task

“…The most common interpretation of this evidence is that distinct systems mediate declarative and implicit forms of learning and memory (Squire and Zola 1996;Cohen et al 1997). Accordingly, the hippocampus would be critically involved in learning and memory if, and only if, conscious awareness of the contingencies occurs (Clark and Squire 1998;Reed and Squire 1999;Manns and Squire 2001;Smith et al 2006).…”

“…The most common interpretation of this evidence is that distinct systems mediate declarative and implicit forms of learning and memory (Squire and Zola 1996;Cohen et al 1997). Accordingly, the hippocampus would be critically involved in learning and memory if, and only if, conscious awareness of the contingencies occurs (Clark and Squire 1998;Reed and Squire 1999;Manns and Squire 2001;Smith et al 2006).While there is no meaningful dispute that the hippocampus is required for conscious learning and memory formation, it may serve a broader function. Several studies have been recently published suggesting that the hippocampus is also implicated in certain implicit tasks (Chun and Phelps 1999;Ryan et al 2000;Greene et al 2006).…”

“…Several studies have been recently published suggesting that the hippocampus is also implicated in certain implicit tasks (Chun and Phelps 1999;Ryan et al 2000;Greene et al 2006). However, for some of these tasks there is controversy about whether they are indeed implicit tasks (Smith and Squire 2005;Smith et al 2006;Greene 2007), while for others there is controversy as to whether the task depends upon the hippocampus (Manns and Squire 2001).In the contextual cueing task (Chun and Jiang 1998), context-dependent target search is impaired in MTL amnesics but does not depend upon recognition (Chun and Phelps 1999). An array of distractors provides a unique context that determines the target (rotated "T") location (see Fig.…”