Experience-Dependent Eye Movements, Awareness, and

Hippocampus-Dependent Memory

Christine N. Smith, Ramona O. Hopkins, and Larry R. Squire

The Journal of NeuroscienceVolume 26, Issue 44, November 1, Pages 11304 -11312

Purpose:Purpose:

What kind of memory is operating when What kind of memory is operating when eye movements change as a result of eye movements change as a result of experience?experience?

Background:Background:

Memory is composed of distinct abilities Memory is composed of distinct abilities that depend on different brain systemsthat depend on different brain systems

Eye movements are signs of behavior that Eye movements are signs of behavior that are measured and correlate with different are measured and correlate with different types of memorytypes of memory

Declarative vs. Implicit memoryDeclarative vs. Implicit memory

3 Experiments To Test:3 Experiments To Test:

1. If eye movements are influenced (changed) 1. If eye movements are influenced (changed) by experience memoryby experience memory

2. If eye movements reflect either conscious 2. If eye movements reflect either conscious or unconscious awarenessor unconscious awareness

3. If this type of identified memory and 3. If this type of identified memory and awareness is hippocampus dependent (relies awareness is hippocampus dependent (relies on this brain system)on this brain system)

Design:Design:

Participants viewed scenes that were either: Participants viewed scenes that were either: novel, repeated, or manipulatednovel, repeated, or manipulated 3 blocks (each with 24 images, 5s/image)3 blocks (each with 24 images, 5s/image) memory test for awarenessmemory test for awareness

E1 & E2: measured eye movements E1 & E2: measured eye movements fixations & scanning of critical regionsfixations & scanning of critical regions

E3: tested amnesic patients ability to correctly E3: tested amnesic patients ability to correctly identify novel, repeated or manipulated imagesidentify novel, repeated or manipulated images measured confidence ratingmeasured confidence rating

SubjectsSubjects

E1: 20 undergraduates; 16F, 4ME1: 20 undergraduates; 16F, 4M

E2: 20 undergraduates; 8F, 12ME2: 20 undergraduates; 8F, 12M

E3: 5 memory impaired patients; 4M, 1F E3: 5 memory impaired patients; 4M, 1F (bilateral lesions to the hippocampus) & 10 (bilateral lesions to the hippocampus) & 10 volunteers (controls); 7M, 4Fvolunteers (controls); 7M, 4F

Materials:Materials: Binocular Apparatus: Head-rest viewpoint eye Binocular Apparatus: Head-rest viewpoint eye

tracker (30hz) & PC-60 software (that detects tracker (30hz) & PC-60 software (that detects pupillary position, measured fixations)pupillary position, measured fixations) Fixations: scored as >100ms elapsed without a Fixations: scored as >100ms elapsed without a

saccade (eye movement of 0.7saccade (eye movement of 0.700 within 33ms) within 33ms)

Position was measured by a 4X4 grid that was Position was measured by a 4X4 grid that was superimposed on image following the experimentsuperimposed on image following the experiment

Results:Results:

Eye movements did differ depending on past Eye movements did differ depending on past viewing of scenes in E1 & E2, specifically simple viewing of scenes in E1 & E2, specifically simple repetitions of an image are sufficient to change repetitions of an image are sufficient to change behavior behavior

Findings were similar in E1 and E2, despite the Findings were similar in E1 and E2, despite the differences in when awareness was assesseddifferences in when awareness was assessed

Impaired performance on memory task & a Impaired performance on memory task & a decrease in confidence in responses of memory decrease in confidence in responses of memory impaired patients in E3impaired patients in E3

E1: block 2E1: block 2

E1: block 3E1: block 3

E2: yielded similar results to E1E2: yielded similar results to E1

E3: Performance of memory E3: Performance of memory impaired patientsimpaired patients

Conclusions:Conclusions:

Eye movements change as a function of experienceEye movements change as a function of experience

Eye movements could not reveal unconscious forms Eye movements could not reveal unconscious forms of memory, thus eye movements reflected conscious of memory, thus eye movements reflected conscious declarative memory for what scenes were novel & declarative memory for what scenes were novel & repeated, and manipulatedrepeated, and manipulated

Ability to classify images correctly & confidently relies Ability to classify images correctly & confidently relies on hippocampus-dependent, declarative memoryon hippocampus-dependent, declarative memory

Bottom Line:Bottom Line:

Experience-dependent eye movements in Experience-dependent eye movements in response to altered scenes reflect response to altered scenes reflect conscious, declarative memory that conscious, declarative memory that supports the link between:supports the link between: Aware (conscious) MemoryAware (conscious) Memory Declarative Memory &Declarative Memory & Hippocampus-dependent MemoryHippocampus-dependent Memory