Synchronized electrical stimulation of the rat medial forebrain bundle and perforant pathway generates an additive BOLD response in the nucleus accumbens and prefrontal cortex

Karla Krautwald, Hoon Ki Min, Kendall H Lee, Frank Angenstein

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

To study how a synchronized activation of two independent pathways affects the fMRI response in a common targeted brain region, blood oxygen dependent (BOLD) signals were measured during electrical stimulation of the right medial forebrain bundle (MFB), the right perforant pathway (PP) and concurrent stimulation of the two fiber systems. Repetitive electrical stimulations of the MFB triggered significant positive BOLD responses in the nucleus accumbens (NAcc), septum, anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC), ventral tegmental area/substantia nigra (VTA/SN), right entorhinal cortex (EC) and colliculus superior, which, in general, declined during later stimulation trains. At the same time, negative BOLD responses were observed in the striatum. Thus, the same stimulus caused region-specific hemodynamic responses. An identical electrical stimulation of the PP generated positive BOLD responses in the right dentate gyrus/hippocampus proper/subiculum (DG/HC), the right entorhinal cortex and the left entorhinal cortex, which remained almost stable during consecutive stimulation trains. Co-stimulation of the two fiber systems resulted in an additive activation pattern, i.e., the BOLD responses were stronger during the stimulation of the two pathways than during the stimulation of only one pathway. However, during the simultaneous stimulation of the two pathways, the development of the BOLD responses to consecutive trains changed. The BOLD responses in regions that were predominantly activated by MFB stimulation (i.e., NAcc, septum and ACC/mPFC) did not decline as fast as during pure MFB stimulation, thus an additive BOLD response was only observed during later trains. In contrast, in the brain regions that were predominantly activated by PP stimulation (i.e., right EC, DG/HC), co-stimulation of the MFB only resulted in an additive effect during early trains but not later trains. Consequently, the development of the BOLD responses during consecutive stimulations indicates the presence of an interaction between the two pathways in a target region, whereas the observed averaged BOLD responses do not.

Original languageEnglish (US)
Pages (from-to)14-25
Number of pages12
JournalNeuroImage
Volume77
DOIs
StatePublished - Aug 5 2013

Fingerprint

Medial Forebrain Bundle
Perforant Pathway
Nucleus Accumbens
Prefrontal Cortex
Entorhinal Cortex
Electric Stimulation
Hippocampus
Parahippocampal Gyrus
Gyrus Cinguli
Dentate Gyrus
Ventral Tegmental Area
Superior Colliculi
Brain
Substantia Nigra
Hemodynamics
Magnetic Resonance Imaging
Oxygen

Keywords

  • Dopamine
  • Electrochemistry
  • Electrophysiology
  • FMRI
  • Hippocampus
  • Nucleus accumbens
  • VTA

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Neurology

Cite this

Synchronized electrical stimulation of the rat medial forebrain bundle and perforant pathway generates an additive BOLD response in the nucleus accumbens and prefrontal cortex. / Krautwald, Karla; Min, Hoon Ki; Lee, Kendall H; Angenstein, Frank.

In: NeuroImage, Vol. 77, 05.08.2013, p. 14-25.

Research output: Contribution to journalArticle

@article{97b3aa0f6c9a473ba325e32a58a34c27,
title = "Synchronized electrical stimulation of the rat medial forebrain bundle and perforant pathway generates an additive BOLD response in the nucleus accumbens and prefrontal cortex",
abstract = "To study how a synchronized activation of two independent pathways affects the fMRI response in a common targeted brain region, blood oxygen dependent (BOLD) signals were measured during electrical stimulation of the right medial forebrain bundle (MFB), the right perforant pathway (PP) and concurrent stimulation of the two fiber systems. Repetitive electrical stimulations of the MFB triggered significant positive BOLD responses in the nucleus accumbens (NAcc), septum, anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC), ventral tegmental area/substantia nigra (VTA/SN), right entorhinal cortex (EC) and colliculus superior, which, in general, declined during later stimulation trains. At the same time, negative BOLD responses were observed in the striatum. Thus, the same stimulus caused region-specific hemodynamic responses. An identical electrical stimulation of the PP generated positive BOLD responses in the right dentate gyrus/hippocampus proper/subiculum (DG/HC), the right entorhinal cortex and the left entorhinal cortex, which remained almost stable during consecutive stimulation trains. Co-stimulation of the two fiber systems resulted in an additive activation pattern, i.e., the BOLD responses were stronger during the stimulation of the two pathways than during the stimulation of only one pathway. However, during the simultaneous stimulation of the two pathways, the development of the BOLD responses to consecutive trains changed. The BOLD responses in regions that were predominantly activated by MFB stimulation (i.e., NAcc, septum and ACC/mPFC) did not decline as fast as during pure MFB stimulation, thus an additive BOLD response was only observed during later trains. In contrast, in the brain regions that were predominantly activated by PP stimulation (i.e., right EC, DG/HC), co-stimulation of the MFB only resulted in an additive effect during early trains but not later trains. Consequently, the development of the BOLD responses during consecutive stimulations indicates the presence of an interaction between the two pathways in a target region, whereas the observed averaged BOLD responses do not.",
keywords = "Dopamine, Electrochemistry, Electrophysiology, FMRI, Hippocampus, Nucleus accumbens, VTA",
author = "Karla Krautwald and Min, {Hoon Ki} and Lee, {Kendall H} and Frank Angenstein",
year = "2013",
month = "8",
day = "5",
doi = "10.1016/j.neuroimage.2013.03.046",
language = "English (US)",
volume = "77",
pages = "14--25",
journal = "NeuroImage",
issn = "1053-8119",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Synchronized electrical stimulation of the rat medial forebrain bundle and perforant pathway generates an additive BOLD response in the nucleus accumbens and prefrontal cortex

AU - Krautwald, Karla

AU - Min, Hoon Ki

AU - Lee, Kendall H

AU - Angenstein, Frank

PY - 2013/8/5

Y1 - 2013/8/5

N2 - To study how a synchronized activation of two independent pathways affects the fMRI response in a common targeted brain region, blood oxygen dependent (BOLD) signals were measured during electrical stimulation of the right medial forebrain bundle (MFB), the right perforant pathway (PP) and concurrent stimulation of the two fiber systems. Repetitive electrical stimulations of the MFB triggered significant positive BOLD responses in the nucleus accumbens (NAcc), septum, anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC), ventral tegmental area/substantia nigra (VTA/SN), right entorhinal cortex (EC) and colliculus superior, which, in general, declined during later stimulation trains. At the same time, negative BOLD responses were observed in the striatum. Thus, the same stimulus caused region-specific hemodynamic responses. An identical electrical stimulation of the PP generated positive BOLD responses in the right dentate gyrus/hippocampus proper/subiculum (DG/HC), the right entorhinal cortex and the left entorhinal cortex, which remained almost stable during consecutive stimulation trains. Co-stimulation of the two fiber systems resulted in an additive activation pattern, i.e., the BOLD responses were stronger during the stimulation of the two pathways than during the stimulation of only one pathway. However, during the simultaneous stimulation of the two pathways, the development of the BOLD responses to consecutive trains changed. The BOLD responses in regions that were predominantly activated by MFB stimulation (i.e., NAcc, septum and ACC/mPFC) did not decline as fast as during pure MFB stimulation, thus an additive BOLD response was only observed during later trains. In contrast, in the brain regions that were predominantly activated by PP stimulation (i.e., right EC, DG/HC), co-stimulation of the MFB only resulted in an additive effect during early trains but not later trains. Consequently, the development of the BOLD responses during consecutive stimulations indicates the presence of an interaction between the two pathways in a target region, whereas the observed averaged BOLD responses do not.

AB - To study how a synchronized activation of two independent pathways affects the fMRI response in a common targeted brain region, blood oxygen dependent (BOLD) signals were measured during electrical stimulation of the right medial forebrain bundle (MFB), the right perforant pathway (PP) and concurrent stimulation of the two fiber systems. Repetitive electrical stimulations of the MFB triggered significant positive BOLD responses in the nucleus accumbens (NAcc), septum, anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC), ventral tegmental area/substantia nigra (VTA/SN), right entorhinal cortex (EC) and colliculus superior, which, in general, declined during later stimulation trains. At the same time, negative BOLD responses were observed in the striatum. Thus, the same stimulus caused region-specific hemodynamic responses. An identical electrical stimulation of the PP generated positive BOLD responses in the right dentate gyrus/hippocampus proper/subiculum (DG/HC), the right entorhinal cortex and the left entorhinal cortex, which remained almost stable during consecutive stimulation trains. Co-stimulation of the two fiber systems resulted in an additive activation pattern, i.e., the BOLD responses were stronger during the stimulation of the two pathways than during the stimulation of only one pathway. However, during the simultaneous stimulation of the two pathways, the development of the BOLD responses to consecutive trains changed. The BOLD responses in regions that were predominantly activated by MFB stimulation (i.e., NAcc, septum and ACC/mPFC) did not decline as fast as during pure MFB stimulation, thus an additive BOLD response was only observed during later trains. In contrast, in the brain regions that were predominantly activated by PP stimulation (i.e., right EC, DG/HC), co-stimulation of the MFB only resulted in an additive effect during early trains but not later trains. Consequently, the development of the BOLD responses during consecutive stimulations indicates the presence of an interaction between the two pathways in a target region, whereas the observed averaged BOLD responses do not.

KW - Dopamine

KW - Electrochemistry

KW - Electrophysiology

KW - FMRI

KW - Hippocampus

KW - Nucleus accumbens

KW - VTA

UR - http://www.scopus.com/inward/record.url?scp=84876718199&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84876718199&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2013.03.046

DO - 10.1016/j.neuroimage.2013.03.046

M3 - Article

C2 - 23558098

AN - SCOPUS:84876718199

VL - 77

SP - 14

EP - 25

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -