Perforant pathway stimulation as a conditioned stimulus for active avoidance learning triggers BOLD responses in various target regions of the hippocampus: A combined fMRI and electrophysiological study

Angenstein, Frank; Krautwald, Karla; Wetzel, Wolfram; Scheich, Henning

doi:10.1016/j.neuroimage.2013.03.007

Cited by 13 publications

(11 citation statements)

References 20 publications

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“…By stimulating the perforant pathway in rodents, functional imaging shows spread BOLD activity in hippocampal formation, entorhinal cortex, prefrontal cortex, cingulate cortex, nucleus accumbens, etc, which supports the involvement of a large-scale cortical-hippocampal network in learning (Angenstein et al, 2013;Canals et al, 2009). Especially, the elevated network response days after repeated stimulation or active avoidance learning suggests that BOLD signal can reflect network efficacy change after learning (Angenstein et al, 2013), which is consistent with our observation of increased resting synchrony of the network after maze learning. In fact, ongoing and propagating synchronous activity in hippocampus, prefrontal cortex and entorhinal cortex after memory encoding has been considered as a mechanism of memory consolidation (Battaglia et al, 2011).…”

Section: Accepted Manuscriptmentioning

confidence: 75%

Functional connectivity MRI tracks memory networks after maze learning in rodents

Nasrallah

Chen

et al. 2016

NeuroImage

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Section: Accepted Manuscriptmentioning

confidence: 75%

Functional connectivity MRI tracks memory networks after maze learning in rodents

Nasrallah

Chen

et al. 2016

NeuroImage

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“…To study the influence of dopaminergic transmission on the BOLD signals in mPFC/ACC and NAcc two related perforant pathway stimulation protocols were applied: a continuous and a discontinuous 100 Hz pulse protocol. 11,17 Both protocols reliably induce BOLD responses in mPFC/ACC and NAcc, but differ in their ability to generate significant BOLD responses in the VTA/SN region. Only the continuous stimulation protocol triggered significant BOLD responses in the VTA/SN region.…”

Section: Resultsmentioning

confidence: 99%

The role of the mesolimbic dopamine system in the formation of blood-oxygen-level dependent responses in the medial prefrontal/anterior cingulate cortex during high-frequency stimulation of the rat perforant pathway

Helbing

Brocka

Scherf

et al. 2016

J Cereb Blood Flow Metab

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Several human functional magnetic resonance imaging studies point to an activation of the mesolimbic dopamine system during reward, addiction and learning. We previously found activation of the mesolimbic system in response to continuous but not to discontinuous perforant pathway stimulation in an experimental model that we now used to investigate the role of dopamine release for the formation of functional magnetic resonance imaging responses. The two stimulation protocols elicited blood-oxygen-level dependent responses in the medial prefrontal/anterior cingulate cortex and nucleus accumbens. Inhibition of dopamine D receptors abolished the formation of functional magnetic resonance imaging responses in the medial prefrontal/anterior cingulate cortex during continuous but not during discontinuous pulse stimulations, i.e. only when the mesolimbic system was activated. Direct electrical or optogenetic stimulation of the ventral tegmental area caused strong dopamine release but only electrical stimulation triggered significant blood-oxygen level-dependent responses in the medial prefrontal/anterior cingulate cortex and nucleus accumbens. These functional magnetic resonance imaging responses were not affected by the D receptor antagonist SCH23390 but reduced by the N-methyl-D-aspartate receptor antagonist MK801. Therefore, glutamatergic ventral tegmental area neurons are already sufficient to trigger blood-oxygen-level dependent responses in the medial prefrontal/anterior cingulate cortex and nucleus accumbens. Although dopamine release alone does not affect blood-oxygen-level dependent responses it can act as a switch, permitting the formation of blood-oxygen-level dependent responses.

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“…The group of Angenstein et al . has previously investigated the relationship between the hippocampal BOLD response patterns and the electrical stimulation patterns at the perforant pathway 14–17 . Two other groups have reported the expansion of the hippocampal BOLD responses to other regions after LTP 18,19 .…”

Section: Introductionmentioning

confidence: 99%

Spatial contribution of hippocampal BOLD activation in high-resolution fMRI

Abe

Tsurugizawa

Bihan

et al. 2019

Sci Rep

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While the vascular origin of the BOLD-fMRI signal is established, the exact neurovascular coupling events contributing to this signal are still incompletely understood. Furthermore, the hippocampal spatial properties of the BOLD activation are not elucidated, although electrophysiology approaches have already revealed the precise spatial patterns of neural activity. High magnetic field fMRI offers improved contrast and allows for a better correlation with the underlying neuronal activity because of the increased contribution to the BOLD signal of small blood vessels. Here, we take advantage of these two benefits to investigate the spatial characteristics of the hippocampal activation in a rat model before and after changing the hippocampal plasticity by long-term potentiation (LTP). We found that the hippocampal BOLD signals evoked by electrical stimulation at the perforant pathway increased more at the radiatum layer of the hippocampal CA1 region than at the pyramidal cell layer. The return to the baseline of the hippocampal BOLD activation was prolonged after LTP induction compared with that before most likely due vascular or neurovascular coupling changes. Based on these results, we conclude that high resolution BOLD-fMRI allows the segregation of hippocampal subfields probably based on their underlying vascular or neurovascular coupling features.

show abstract

Perforant pathway stimulation as a conditioned stimulus for active avoidance learning triggers BOLD responses in various target regions of the hippocampus: A combined fMRI and electrophysiological study

Cited by 13 publications

References 20 publications

Functional connectivity MRI tracks memory networks after maze learning in rodents

Functional connectivity MRI tracks memory networks after maze learning in rodents

The role of the mesolimbic dopamine system in the formation of blood-oxygen-level dependent responses in the medial prefrontal/anterior cingulate cortex during high-frequency stimulation of the rat perforant pathway

Spatial contribution of hippocampal BOLD activation in high-resolution fMRI

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