The Eyes Remember It: Oculography and Pupillometry during Recollection in Three Amnesic Patients

Two patients (TC and SS) with lesions that included the hippocampal regions (predominantly on the left side) were severely impaired in their recall of simple, verbally stated facts. However, both patients remembered spatial information that was temporally associated with semantic information. Specifically, TC and SS could not recall explicitly the content of an episode, but their spontaneous oculomotor behavior showed that they retained some information about the event as their gaze automatically returned to the locations on the computer screen where visual information had been paired to verbally presented information. Thus, this spatial information is implicit, automatically retrieved, and eye-based, as when one patient (TC) was asked to point with the finger to the same positions he was impaired. In addition, in an old/new recognition task, TC and SS and an additional patient, OB, showed significant changes in eye pupil diameter when viewing novel visual stimuli compared to stimuli that they had previously seen, also when they (incorrectly) declared with confidence that an old item was new. The spared memory of these patients, despite severe amnesia for the learning episodes, is characterized by a re-enactment of previous eye fixations that were associated with each (forgotten) episode and physiological responses (as indexed by pupillometry) to previously seen stimuli. Such spared memory can be seen as a type of “snapshot” memory, which automatically processes eye-based spatial information and whose content remains implicit. Finally, we surmise on the basis of the neuroanatomical findings of these patients, that neural substrates in the spared (right) hemisphere might support both the eye fixations' re-enactment and implicit visual pattern recognition.