The current functional state of local neuronal circuits controls the magnitude of a BOLD response to incoming stimuli

Angenstein, Frank; Krautwald, Karla; Scheich, Henning

doi:10.1016/j.neuroimage.2010.01.070

Cited by 29 publications

(32 citation statements)

References 27 publications

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“…dentate gyrus, hippocampus proper, subiculum, and entorhinal cortex; Fig. 2A), as has been observed and reported in previous experiments (Angenstein et al, 2010). The generated BOLD responses in the DG/hippocampus proper to successive stimulation trains differed significantly (ANOVA: F = 15.8; df = 7; p b 0.001; n rat = 8;).…”

Section: Bold Responses During Short and Long Burst Stimulationsupporting

confidence: 87%

Variations in the temporal pattern of perforant pathway stimulation control the activity in the mesolimbic pathway

2013

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Section: Bold Responses During Short and Long Burst Stimulationsupporting

confidence: 87%

Variations in the temporal pattern of perforant pathway stimulation control the activity in the mesolimbic pathway

2013

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“…High stimulation intensities resulted in significant fEPSP-LTP. The involvement of just a small neuronal population in the processing of the specific information, as suggested by optogenetic studies (Miesenböck 2009), may explain our results: By stimulation of a smaller number of synapses through low intensity test pulses (Angenstein et al 2010) as in our case, the higher proportion of silenced memory related synapses can reduce or even impair the observed field potential. After high-intensity stimulation, as in the Jeffery (1995) study, the silencing of these synapses is masked by potentiation of a higher number of memory-unrelated synapses, thus resulting in higher fEPSP.…”

Section: Discussionsupporting

confidence: 66%

Emotional and cognitive information processing: Relations to behavioral performance and hippocampal long-term potentiation in vivo during a spatial water maze training in rats

Schulz¹,

Korz²

2010

Learn. Mem.

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Emotionality as well as cognitive abilities contribute to the acquisition and retrieval of memories as well as to the consolidation of long-term potentiation (LTP), a cellular model of memory formation. However, little is known about the timescale and relative contribution of these processes. Therefore, we tested the effects of weak water maze training, containing both emotional and cognitive demands, on LTP in the hippocampal dentate gyrus. The population spike amplitude (PSA)-LTP was prolonged in all rats irrespective of whether they memorized the platform position or not, whereas the field excitatory postsynaptic potential (fEPSP)-LTP was impaired in good learners and enhanced in poor learners. We then dissociated the behavioral performance of rats during the water maze task by principal component analysis and by means of stress hormone concentrations into underlying "emotional" and "cognitive" factors. PSA-LTP was associated with "emotional" and fEPSP-LTP with "cognitive" behavior. PSA-LTP was depotentiated after the blockade of corticosterone binding mineralocorticoid receptors (MRs) in trained animals, while fEPSP-LTP was unaffected. These results suggest that synaptic processing and encoding of emotional information in the hippocampal dentate gyrus is realized fast and further information transfer is detectable by the reinforcement of PSA-LTP, whereas that of cognitive memories is long lasting.Memory is formed and stored quickly when supported by concurrent emotional experience, whereas the formation of cognitive memories requires repeated training and occurs at a longer timescale (Fanselow 2000;Shors 2001;Sapolsky 2003;Frank et al. 2004). Long-term potentiation (LTP), a cellular model of memory formation, can be dissociated into a short-lived, protein synthesis-independent form (early LTP) and a prolonged, protein synthesis-dependent form (late LTP). The electrically induced early form can be reinforced (consolidated) into the late form by emotional or cognitive stimuli temporally related to the time point of LTP induction (Seidenbecher et al. 1997; Frey 2003, 2004).As emotional and cognitive memories are stored at different timescales, the effective time windows for LTP consolidation induced by emotional and cognitive stimuli may also vary. In the literature LTP and its modulation by memory processes is mostly measured as the field excitatory postsynaptic potential (fEPSP), i.e., the efficacy of synaptic communication between neurons. However, if emotional memories are quickly established, fEPSP-LTP may be affected only during a very short time period after the emotional stimulus. This is supported by recent in vitro findings (Fonseca et al. 2006) which show that the induction and maintenance (30 min to 1 h) of an early fEPSP-LTP can also, in dependence on neuronal activity, be protein synthesis dependent. Thus, during emotional demands with high neuronal activity the memory network may be established rapidly by such mechanisms. An already established memory network may, over time, be better detectable...

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“…Whereas during low intensity stimulation, the time courses of BOLD responses were similar between all three stimulation blocks, the time courses varied during high intensity stimulation ( Figure 2C). As shown previously, the functional properties of dentate neuronal circuits change during the first high intensity stimulation trains (Angenstein et al, 2010). Consequently, the conditions that lead to BOLD responses in the second and third stimulation blocks are highly representative of this altered state.…”

Section: N-methyl-d-aspartate Receptor Inhibition Modifies the Blood supporting

confidence: 55%

“…Therefore, the magnitude of the BOLD response to these low intensity stimulation trains can be used as a comparative parameter for the BOLD response to subsequent high intensity stimulation trains. As described previously, BOLD responses to low intensity stimulation trains become reduced when high intensity stimulation trains are inserted (Angenstein et al, 2010). To check whether this effect depends on NMDA-dependent mechanisms, we added a third stimulation block containing identical low intensity stimulation trains.…”

Section: Effect Of Mk801 Applied Immediately Before Repetitive Stimulmentioning

confidence: 99%

NMDA-Dependent Mechanisms Only Affect the BOLD Response in the Rat Dentate Gyrus by Modifying Local Signal Processing

Tiede

Krautwald

Fincke

et al. 2011

J Cereb Blood Flow Metab

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The role of N-methyl-D-aspartate (NMDA) receptor-mediated mechanisms in the formation of a blood oxygen level-dependent (BOLD) response was studied using electrical stimulation of the right perforant pathway. Stimulation of this fiber bundle triggered BOLD responses in the right hippocampal formation and in the left entorhinal cortex. The perforant pathway projects to and activates the dentate gyrus monosynaptically, activation in the contralateral entorhinal cortex is multisynaptic and requires forwarding and processing of signals. Application of the NMDA receptor antagonist MK801 during stimulation had no effect on BOLD responses in the right dentate gyrus, but reduced the BOLD responses in the left entorhinal cortex. In contrast, application of MK801 before the first stimulation train reduced the BOLD response in both regions. Electrophysiological recordings revealed that the initial stimulation trains changed the local processing of the incoming signals in the dentate gyrus. This altered electrophysiological response was not further changed by a subsequent application of MK801, which is in agreement with an unchanged BOLD response. When MK801 was present during the first stimulation train, a dissimilar electrophysiological response pattern was observed and corresponds to an altered BOLD response, indicating that NMDA-dependent mechanisms indirectly affect the BOLD response, mainly via modifying local signal processing and subsequent propagation.

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The current functional state of local neuronal circuits controls the magnitude of a BOLD response to incoming stimuli

Cited by 29 publications

References 27 publications

Variations in the temporal pattern of perforant pathway stimulation control the activity in the mesolimbic pathway

Variations in the temporal pattern of perforant pathway stimulation control the activity in the mesolimbic pathway

Emotional and cognitive information processing: Relations to behavioral performance and hippocampal long-term potentiation in vivo during a spatial water maze training in rats

NMDA-Dependent Mechanisms Only Affect the BOLD Response in the Rat Dentate Gyrus by Modifying Local Signal Processing

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