Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory

Jon R. Law, Marci A. Flanery, Sylvia Wirth, Marianna Yanike, Anne C. Smith, Loren M. Frank, Wendy Suzuki, Emery N. Brown, Craig E L Stark

Research output: Contribution to journalArticle

Abstract

Recent neurophysiological findings from the monkey hippocampus showed dramatic changes in the firing rate of individual hippocampal cells as a function of learning new associations. To extend these findings to humans, we used blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine the patterns of brain activity during learning of an analogous associative task. We observed bilateral, monotonic increases in activity during learning not only in the hippocampus but also in the parahippocampal and right perirhinal cortices. In addition, activity related to simple novelty signals was observed throughout the medial temporal lobe (MTL) memory system and in several frontal regions. A contrasting pattern was observed in a frontoparietal network in which a high level of activity was sustained until the association was well learned, at which point the activity decreased to baseline. Thus, we found that associative learning in humans is accompanied by striking increases in BOLD fMRI activity throughout the MTL as well as in the cingulate cortex and frontal lobe, consistent with neurophysiological findings in the monkey hippocampus. The finding that both the hippocampus and surrounding MTL cortex exhibited similar associative learning and novelty signals argues strongly against the view that there is a clear division of labor in the MTL in which the hippocampus is essential for forming associations and the cortex is involved in novelty detection. A second experiment addressed a striking aspect of the data from the first experiment by demonstrating a substantial effect of baseline task difficulty on MTL activity capable of rendering mnemonic activity as either "positive" or "negative."

Original languageEnglish (US)
Pages (from-to)5720-5729
Number of pages10
JournalJournal of Neuroscience
Volume25
Issue number24
DOIs
StatePublished - Jun 15 2005

Fingerprint

Temporal Lobe
Magnetic Resonance Imaging
Hippocampus
Learning
Haplorhini
Association Learning
Gyrus Cinguli
Frontal Lobe
Brain

Keywords

  • Associative
  • Declarative
  • Explicit
  • Hippocampus
  • Medial temporal lobe
  • Recollection

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Law, J. R., Flanery, M. A., Wirth, S., Yanike, M., Smith, A. C., Frank, L. M., ... Stark, C. E. L. (2005). Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. Journal of Neuroscience, 25(24), 5720-5729. https://doi.org/10.1523/JNEUROSCI.4935-04.2005

Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. / Law, Jon R.; Flanery, Marci A.; Wirth, Sylvia; Yanike, Marianna; Smith, Anne C.; Frank, Loren M.; Suzuki, Wendy; Brown, Emery N.; Stark, Craig E L.

In: Journal of Neuroscience, Vol. 25, No. 24, 15.06.2005, p. 5720-5729.

Research output: Contribution to journalArticle

Law, Jon R. ; Flanery, Marci A. ; Wirth, Sylvia ; Yanike, Marianna ; Smith, Anne C. ; Frank, Loren M. ; Suzuki, Wendy ; Brown, Emery N. ; Stark, Craig E L. / Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. In: Journal of Neuroscience. 2005 ; Vol. 25, No. 24. pp. 5720-5729.
@article{2ea772c522024d78ad64c20e9f69a2cc,
title = "Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory",
abstract = "Recent neurophysiological findings from the monkey hippocampus showed dramatic changes in the firing rate of individual hippocampal cells as a function of learning new associations. To extend these findings to humans, we used blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine the patterns of brain activity during learning of an analogous associative task. We observed bilateral, monotonic increases in activity during learning not only in the hippocampus but also in the parahippocampal and right perirhinal cortices. In addition, activity related to simple novelty signals was observed throughout the medial temporal lobe (MTL) memory system and in several frontal regions. A contrasting pattern was observed in a frontoparietal network in which a high level of activity was sustained until the association was well learned, at which point the activity decreased to baseline. Thus, we found that associative learning in humans is accompanied by striking increases in BOLD fMRI activity throughout the MTL as well as in the cingulate cortex and frontal lobe, consistent with neurophysiological findings in the monkey hippocampus. The finding that both the hippocampus and surrounding MTL cortex exhibited similar associative learning and novelty signals argues strongly against the view that there is a clear division of labor in the MTL in which the hippocampus is essential for forming associations and the cortex is involved in novelty detection. A second experiment addressed a striking aspect of the data from the first experiment by demonstrating a substantial effect of baseline task difficulty on MTL activity capable of rendering mnemonic activity as either {"}positive{"} or {"}negative.{"}",
keywords = "Associative, Declarative, Explicit, Hippocampus, Medial temporal lobe, Recollection",
author = "Law, {Jon R.} and Flanery, {Marci A.} and Sylvia Wirth and Marianna Yanike and Smith, {Anne C.} and Frank, {Loren M.} and Wendy Suzuki and Brown, {Emery N.} and Stark, {Craig E L}",
year = "2005",
month = "6",
day = "15",
doi = "10.1523/JNEUROSCI.4935-04.2005",
language = "English (US)",
volume = "25",
pages = "5720--5729",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "24",

}

TY - JOUR

T1 - Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory

AU - Law, Jon R.

AU - Flanery, Marci A.

AU - Wirth, Sylvia

AU - Yanike, Marianna

AU - Smith, Anne C.

AU - Frank, Loren M.

AU - Suzuki, Wendy

AU - Brown, Emery N.

AU - Stark, Craig E L

PY - 2005/6/15

Y1 - 2005/6/15

N2 - Recent neurophysiological findings from the monkey hippocampus showed dramatic changes in the firing rate of individual hippocampal cells as a function of learning new associations. To extend these findings to humans, we used blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine the patterns of brain activity during learning of an analogous associative task. We observed bilateral, monotonic increases in activity during learning not only in the hippocampus but also in the parahippocampal and right perirhinal cortices. In addition, activity related to simple novelty signals was observed throughout the medial temporal lobe (MTL) memory system and in several frontal regions. A contrasting pattern was observed in a frontoparietal network in which a high level of activity was sustained until the association was well learned, at which point the activity decreased to baseline. Thus, we found that associative learning in humans is accompanied by striking increases in BOLD fMRI activity throughout the MTL as well as in the cingulate cortex and frontal lobe, consistent with neurophysiological findings in the monkey hippocampus. The finding that both the hippocampus and surrounding MTL cortex exhibited similar associative learning and novelty signals argues strongly against the view that there is a clear division of labor in the MTL in which the hippocampus is essential for forming associations and the cortex is involved in novelty detection. A second experiment addressed a striking aspect of the data from the first experiment by demonstrating a substantial effect of baseline task difficulty on MTL activity capable of rendering mnemonic activity as either "positive" or "negative."

AB - Recent neurophysiological findings from the monkey hippocampus showed dramatic changes in the firing rate of individual hippocampal cells as a function of learning new associations. To extend these findings to humans, we used blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine the patterns of brain activity during learning of an analogous associative task. We observed bilateral, monotonic increases in activity during learning not only in the hippocampus but also in the parahippocampal and right perirhinal cortices. In addition, activity related to simple novelty signals was observed throughout the medial temporal lobe (MTL) memory system and in several frontal regions. A contrasting pattern was observed in a frontoparietal network in which a high level of activity was sustained until the association was well learned, at which point the activity decreased to baseline. Thus, we found that associative learning in humans is accompanied by striking increases in BOLD fMRI activity throughout the MTL as well as in the cingulate cortex and frontal lobe, consistent with neurophysiological findings in the monkey hippocampus. The finding that both the hippocampus and surrounding MTL cortex exhibited similar associative learning and novelty signals argues strongly against the view that there is a clear division of labor in the MTL in which the hippocampus is essential for forming associations and the cortex is involved in novelty detection. A second experiment addressed a striking aspect of the data from the first experiment by demonstrating a substantial effect of baseline task difficulty on MTL activity capable of rendering mnemonic activity as either "positive" or "negative."

KW - Associative

KW - Declarative

KW - Explicit

KW - Hippocampus

KW - Medial temporal lobe

KW - Recollection

UR - http://www.scopus.com/inward/record.url?scp=20544439388&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=20544439388&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.4935-04.2005

DO - 10.1523/JNEUROSCI.4935-04.2005

M3 - Article

C2 - 15958738

AN - SCOPUS:20544439388

VL - 25

SP - 5720

EP - 5729

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 24

ER -