Retrieval of Relational Information: A Role for the Left Inferior Prefrontal Cortex

doi:10.1006/nimg.2002.1219

NeuroImage

Volume 17, Issue 1, September 2002, Pages 393-400

https://doi.org/10.1006/nimg.2002.1219 Get rights and content

Abstract

Neuroimagingstudies have implicated different areas of prefrontal cortex and medial temporal lobe structures (MTL) in episodic retrieval tasks. However, the role of specific regions in particular aspects of episodic memory is still unclear. In this experiment we studied changes in regional cerebral blood flow (rCBF) associated with relational and nonrelational retrieval of studied pairs of words. For relational retrieval, a list of either studied or rearranged pairs was presented and subjects (n = 8) were asked to indicate whether pairs had appeared on the study list. Under the nonrelational retrieval condition they indicated whether one or both words of the pair had appeared on the study list. As compared to the baseline condition (looking at a cross-mark), increased rCBF was observed in the left inferior prefrontal cortex (LIPFC) for both studied pairs and rearranged pairs under the relational retrieval condition. Under the nonrelational condition, an increase was observed in right inferior frontal gyrus. The MTL showed a trend for increased rCBF in the rearranged-pair condition. This increase was probably associated with the encoding that accompanies retrieval of novel stimuli. Results suggest that the lateralized activation of prefrontal cortex observed in episodic memory tasks may be related to the degree of relational processing involved. The LIPFC appears to be associated with relational retrieval and the right prefrontal cortex with nonrelational retrieval.

References (61)

K. Allan et al.
The role of the right anterior prefrontal cortex in episodic retrieval
NeuroImage
(2000)
R.D. Badgaiyan et al.
Priming within and across modalities: Exploring the nature of rCBF increases and decreases
NeuroImage
(2001)
T.S. Braver et al.
Direct comparison of prefrontal cortex regions engaged by working and long-term memory tasks
NeuroImage
(2001)
J.T. Coull et al.
A fronto-parietal network for rapid visual information processing: A PET study of sustained attention and working memory
Neuropsychologia
(1996)
S. Dubois et al.
Effect of familiarity on the processing of human faces
NeuroImage
(1999)
G. Fernandez et al.
Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: Human declarative memory formation at the system level
Brain Res. Bull.
(2001)
T.L. Jernigan et al.
Brain activation during word identification and word recognition
NeuroImage
(1998)
N. Kapur et al.
Activation of human hippocampal formation during memory for faces: A PET study
Cortex
(1995)
S. Kohler et al.
Networks of domain-specific and general regions involved in episodic memory for spatial location and object identity
Neuropsychologia
(1998)
M. Lepage et al.
Neural correlates of semantic associative encoding in episodic memory
Brain Res. Cogn. Brain Res.
(2000)

S.F. Nolde et al.

The role of prefrontal cortex during tests of episodic memory

Trends Cogn. Sci.

(1998)

D. Raczkowski et al.

Reliability and validity of some handedness questionnaire items

Neuropsychologia

(1974)

J.D. Ragland et al.

Hemispheric activation of anterior and inferior prefrontal cortex during verbal encoding and recognition: A PET study of healthy volunteers

NeuroImage

(2000)

M.D. Rugg et al.

The role of the prefrontal cortex in recognition memory and memory for source: An fMRI study

NeuroImage

(1999)

G.R. Savage et al.

Direct and indirect measures of verbal relational memory following anterior temporal lobectomy

Neuropsychologia

(2002)

E.E. Smith et al.

Working memory: A view from neuroimaging

Cogn. Psychol.

(1997)

P. Alvarez et al.

Differential effects of damage within the hippocampal region on memory for a natural, nonspatial odor-odor association

Learn Mem.

(2001)

R.D. Badgaiyan

Neuroanatomical organization of perceptual memory: An fMRI study of picture priming

Hum. Brain Mapp.

(2000)

R.D. Badgaiyan et al.

Time course of cortical activations in implicit and explicit recall

J. Neurosci.

(1997)

R.D. Badgaiyan et al.

Auditory priming within and across modalities: Evidence from positron emission tomography

J. Cogn. Neurosci.

(1999)

Badgaiyan, R. D, Schacter, D. L, and, Alpert, N. M. 2000, Characterization of the nature of cerebral blood flow changes...

R.L. Buckner et al.

Encoding processes during retrieval tasks

J. Cogn. Neurosci.

(2001)

N.J. Cohen et al.

Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that

Science

(1980)

J.B. Demb et al.

Semantic encoding and retrieval in the left inferior prefrontal cortex: A functional MRI study of task difficulty and process specificity

J. Neurosci.

(1995)

R.J. Dolan et al.

Dissociating prefrontal and hippocampal function in episodic memory encoding

Nature

(1997)

H. Eichenbaum

Declarative memory: Insights from cognitive neurobiology

Annu. Rev. Psychol.

(1997)

K.J. Friston et al.

Comparing functional (PET) images: The assessment of significant change

J. Cereb. Blood Flow Metab.

(1991)

K.J. Friston et al.

Statistical parametric maps in functional imaging: A general approach

Hum. Brain Mapp.

(1995)

C. Gerlach et al.

Perceptual differentiation and category effects in normal object recognition: A PET study

Brain

(1999)

K. Henke et al.

Human hippocampus establishes associations in memory

Hippocampus

(1997)

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¹: To whom correspondence should be addressed at Harvard University, William James Hall, Room 875, 33, Kirkland Street, Cambridge, MA 02138. Fax: (617) 496-3122. E-mail: [email protected].

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Regular ArticleRetrieval of Relational Information: A Role for the Left Inferior Prefrontal Cortex

Abstract

NeuroImage

NeuroImage

NeuroImage

Neuropsychologia

NeuroImage

Brain Res. Bull.

NeuroImage

Cortex

Neuropsychologia

Brain Res. Cogn. Brain Res.

Trends Cogn. Sci.

Neuropsychologia

NeuroImage

NeuroImage

Neuropsychologia

Cogn. Psychol.

Differential effects of damage within the hippocampal region on memory for a natural, nonspatial odor-odor association

Learn Mem.

Neuroanatomical organization of perceptual memory: An fMRI study of picture priming

Hum. Brain Mapp.

Time course of cortical activations in implicit and explicit recall

J. Neurosci.

Auditory priming within and across modalities: Evidence from positron emission tomography

J. Cogn. Neurosci.

Encoding processes during retrieval tasks

J. Cogn. Neurosci.

Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that

Science

Semantic encoding and retrieval in the left inferior prefrontal cortex: A functional MRI study of task difficulty and process specificity

J. Neurosci.

Dissociating prefrontal and hippocampal function in episodic memory encoding

Nature

Declarative memory: Insights from cognitive neurobiology

Annu. Rev. Psychol.

Comparing functional (PET) images: The assessment of significant change

J. Cereb. Blood Flow Metab.

Statistical parametric maps in functional imaging: A general approach

Hum. Brain Mapp.

Perceptual differentiation and category effects in normal object recognition: A PET study

Brain

Human hippocampus establishes associations in memory

Hippocampus

Regular Article
Retrieval of Relational Information: A Role for the Left Inferior Prefrontal Cortex