Functional-anatomic correlates of remembering and knowing

doi:10.1016/j.neuroimage.2003.11.001

NeuroImage

Volume 21, Issue 4, April 2004, Pages 1337-1349

https://doi.org/10.1016/j.neuroimage.2003.11.001 Get rights and content

Abstract

Neural correlates of remembering were examined using event-related functional MRI (fMRI) in 20 young adults. A recognition paradigm based on the remember/know (RK) procedure was used to separately classify studied items that were correctly identified and accompanied by a conscious recollection of details about the study episode from studied items that were correctly identified in the absence of conscious recollection. To facilitate exploration of the basis of remember decisions, studied items were paired with pictures and sounds to encourage retrieval of specific content during scanned testing. Analyses using a priori regions of interest indicated that remembering recruited both regions that associate with the perception and/or decision that information is old and regions that associate preferentially with visual content, while knowing recruited regions associated with oldness, but did not recruit visual content regions. Exploratory analyses further indicated a functional dissociation across regions of parietal cortex that may aid to reconcile several divergent results in the literature. Lateral parietal regions responded preferentially to remember decisions, while a slightly medial region responded robustly to both remember and know decisions. Taken collectively, these results suggest that remembering and knowing associate with common processes supporting a perception and/or the decision that information is old. Remembering additionally recruits regions specific to retrieved content, which may participate to convey the vividness typical of recollective experience.

Section snippets

Subjects

Twenty five right-handed subjects from the Washington University community participated. Of these, one was excluded from analysis due to excessive movement during imaging (>1 mm within-run movement), two for failure to comply with task instructions, and three for having an insufficient number of know responses for functional imaging analyses (<9). The remaining 20 subjects (seven females) ranged in age from 18 to 32 years (mean 23 years), had normal or corrected-to-normal vision, were native

Behavioral results

Accuracy and response time (RT) data are listed in Table 1. Subjects correctly recognized 62% of the old items studied with pictures (Table 1). Of those correctly recognized old items, 63% were identified as having been remembered and 37% known. Subjects guessed or made no response on 8% of old and 11% of new items, and correctly rejected 59% of the new lures. FA-REM, FA-KNOW, and GUESS trials with no response were not included in subsequent imaging analyses. Two-tailed t tests showed that

Discussion

The primary findings in this experiment were that remembering and knowing both activated a left intraparietal region that associates with the perception or decision that information is old, and remembering additionally activated content-based anterior fusiform regions that associate with processing visual object information. More specifically, items correctly identified as old corresponded with increased activity in left intraparietal cortex at or near BA 40/39, relative to missed old and

Acknowledgements

We thank Larry Jacoby, Kathleen McDermott, Luigi Maccotta, Fran Miezin, Steve Petersen, Jeff Toth, Endel Tulving, and Katerina Velanova for helpful comments, assistance, and advice. Denise Head assisted with data collection. Avi Snyder helped develop post-processing software and Tom Conturo and Erbil Akbudak supplied imaging sequences. David Van Essen provided Caret software. Two anonymous reviewers provided helpful suggestions. This research was supported by the Howard Hughes Medical

References (103)

R.L Buckner et al.
Functional-anatomic study of episodic retrieval: II. Selective averaging of event-related fMRI trials to test the retrieval success hypothesis
NeuroImage
(1998)
R.L Buckner et al.
Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI
Neuron
(1998)
J.C Culham et al.
Neuroimaging of cognitive functions in human parietal cortex
Curr. Opin. Neurobiol.
(2001)
B Desgranges et al.
The functional neuroanatomy of episodic memory: the role of the frontal lobes, the hippocampal formation, and other areas
NeuroImage
(1998)
I.G Dobbins et al.
Executive control during episodic retrieval: multiple prefrontal processes subserve source memory
Neuron
(2002)
I.G Dobbins et al.
Memory orientation and success: separable neurocognitive components underlying episodic recognition
Neuropsychologia
(2003)
D.I Donaldson et al.
Recognition memory for new associations: electrophysiological evidence for the role of recollection
Neuropsychologia
(1998)
D.I Donaldson et al.
Dissociating memory retrieval processes using fMRI: evidence that priming does not support recognition memory
Neuron
(2001)
D.I Donaldson et al.
Dissociating state and item components of recognition memory using fMRI
NeuroImage
(2001)
M.J Farah
The neural basis of mental imagery
Trends Neurosci.
(1989)

A.Z Snyder

Difference image versus ratio image error function forms in PET–PET realignment

D.C Van Essen et al.

Mapping visual cortex in monkeys and humans using surface-based atlases

Vision Res.

(2001)

A.D Wagner

Working memory contributions to human learning and remembering

Neuron

(1999)

E.L Wilding et al.

Event-related potentials and the recognition memory exclusion task

Neuropsychologia

(1997)

E.L Wilding et al.

Recognition memory with and without retrieval of context: an event-related potential study

Neuropsychologia

(1995)

S.V Astafiev et al.

Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing

J. Neurosci.

(2003)

P.A Bandettini et al.

Processing strategies for time-course data sets in functional MRI of the human brain

Magn. Reson. Med.

(1993)

F.C Bartlett

Remembering: A Study in Experimental and Social Psychology

(1932)

G.M Boynton et al.

Linear systems analysis of functional magnetic resonance imaging in human V1

J. Neurosci.

(1996)

R.L Buckner et al.

The cognitive neuroscience of remembering

Nat. Rev., Neurosci.

(2001)

R.L Buckner et al.

Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming

Brain

(2000)

P.W Burgess et al.

Confabulation and the control of recollection

Memory

(1996)

R Cabeza et al.

Imaging cognition II: an empirical review of 275 PET and fMRI studies

J. Cogn. Neurosci.

(2000)

S Cansino et al.

Brain activity underlying encoding and retrieval of source memory

Cereb. Cortex

(2002)

J.D Cohen et al.

PsyScope: a new graphic interactive environment for designing psychology experiments

Behav. Res. Meth. Instrum. Comput.

(1993)

J.D Connolly et al.

Human fMRI evidence for the neural correlates of preparatory set

Nat. Neurosci.

(2002)

T.E Conturo et al.

Sensitivity optimization and experimental design in functional magnetic resonance imaging

Abstr. - Soc. Neurosci.

(1996)

A.M Dale et al.

Selective averaging of rapidly presented individual trials using fMRI

Hum. Brain Mapp.

(1997)

R Desimone et al.

Multiple memory systems in the visual cortex

M D'Esposito et al.

Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies

Exp. Brain Res.

(2000)

H.A Drury et al.

Computerized mappings of the cerebral cortex. A multiresolution flattening method and a surface-based coordinate system

J. Cogn. Neurosci.

(1996)

E Düzel et al.

Event-related brain potential correlates of two states of conscious awareness in memory

Proc. Natl. Acad. Sci. U. S. A.

(1997)

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Functional-anatomic correlates of remembering and knowing

Abstract

Section snippets

Subjects

Behavioral results

Discussion

Acknowledgements

NeuroImage

Neuron

Curr. Opin. Neurobiol.

NeuroImage

Neuron

Neuropsychologia

Neuropsychologia

Neuron

NeuroImage

Trends Neurosci.

Conscious. Cogn.

Neuron

J. Mem. Lang.

Neuron

Neuropsychologia

NeuroImage

NeuroImage

Neuropsychologia

NeuroImage

NeuroImage

NeuroImage

Neuropsychologia

Trends Cogn. Sci.

NeuroImage

Neuropsychologia

Cogn. Brain Res.

Neuropsychologia

NeuroImage

Vision Res.

Neuron

Neuropsychologia

Neuropsychologia

Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing

J. Neurosci.

Processing strategies for time-course data sets in functional MRI of the human brain

Magn. Reson. Med.

Remembering: A Study in Experimental and Social Psychology

Linear systems analysis of functional magnetic resonance imaging in human V1

J. Neurosci.

The cognitive neuroscience of remembering

Nat. Rev., Neurosci.

Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming

Brain

Confabulation and the control of recollection

Memory

Imaging cognition II: an empirical review of 275 PET and fMRI studies

J. Cogn. Neurosci.

Brain activity underlying encoding and retrieval of source memory

Cereb. Cortex

PsyScope: a new graphic interactive environment for designing psychology experiments

Behav. Res. Meth. Instrum. Comput.

Human fMRI evidence for the neural correlates of preparatory set

Nat. Neurosci.

Sensitivity optimization and experimental design in functional magnetic resonance imaging

Abstr. - Soc. Neurosci.

Selective averaging of rapidly presented individual trials using fMRI

Hum. Brain Mapp.

Multiple memory systems in the visual cortex

Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies

Exp. Brain Res.

Computerized mappings of the cerebral cortex. A multiresolution flattening method and a surface-based coordinate system

J. Cogn. Neurosci.

Event-related brain potential correlates of two states of conscious awareness in memory

Proc. Natl. Acad. Sci. U. S. A.