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Exploring the post-stimulus undershoot with spin-echo fMRI: implications for models of neurovascular response.

ABSTRACT: As a consequence of neural stimulation the blood oxygenation-level dependent (BOLD) contrast in gradient-echo echo-planar imaging (GE-EPI) based functional MRI (fMRI) leads to an increased MR signal in activated brain regions. Following this, a BOLD signal undershoot below baseline is generally observed with GE-EPI. The origin of this undershoot has been the focus of many investigations using fMRI and optical modalities, but the underlying mechanisms remain disputed. Here, we investigate the BOLD undershoot following visual stimulation by using a purely T?-weighted fMRI sequence at 1.5 and 3 T. By taking advantage of the field strength dependency of the T? BOLD contrast and complete absence of static dephasing effects due to the pure spin echoes, one can draw conclusions about the origin of the BOLD undershoot and test the hypotheses in the literature. We observe a significant undershoot at both field strengths, with constant undershoot-to-main response ratio. This provides strong evidence that the undershoot is caused by BOLD changes due to elevated post-stimulus deoxyhaemoglobin concentration in the small vessels. 'Delayed vascular compliance' as suggested by the well-known Balloon and Windkessel models does not appear capable of explaining the undershoot. Our results also suggest that blood volume changes in arterioles and capillaries, for which there is consistent evidence from optical imaging studies, cannot alone cause the undershoot. This has important implications for models of neurovascular response and provides further support for the decoupling of changes in the rate of oxygen metabolism and blood flow. In addition, we found that an 'arteriolar balloon' (delayed arterial compliance) may provide a plausible explanation for the temporal characteristics of the BOLD undershoot.

SUBMITTER: Poser BA

PROVIDER: S-EPMC6869868 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Exploring the post-stimulus undershoot with spin-echo fMRI: implications for models of neurovascular response.

Poser Benedikt A BA van Mierlo Emily E Norris David G DG

Human brain mapping 20110101 1

As a consequence of neural stimulation the blood oxygenation-level dependent (BOLD) contrast in gradient-echo echo-planar imaging (GE-EPI) based functional MRI (fMRI) leads to an increased MR signal in activated brain regions. Following this, a BOLD signal undershoot below baseline is generally observed with GE-EPI. The origin of this undershoot has been the focus of many investigations using fMRI and optical modalities, but the underlying mechanisms remain disputed. Here, we investigate the BOL ...[more]

PMID: 20623748

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Project description:Post-stimulus undershoots, negative responses following cessation of stimulation, are widely observed in functional magnetic resonance (fMRI) blood oxygenation level dependent (BOLD) data. However, the debate surrounding whether the origin of this response phase is neuronal or vascular, and whether it provides functionally relevant information, that is additional to what is contained in the primary response, means that undershoots are widely overlooked. We simultaneously recorded electroencephalography (EEG), BOLD and cerebral blood-flow (CBF) [obtained from arterial spin labelled (ASL) fMRI] fMRI responses to hemifield checkerboard stimulation to test the potential neural origin of the fMRI post-stimulus undershoot. The post-stimulus BOLD and CBF signal amplitudes in both contralateral and ipsilateral visual cortex depended on the post-stimulus power of the occipital 8-13Hz (alpha) EEG neuronal activity, such that trials with highest EEG power showed largest fMRI undershoots in contralateral visual cortex. This correlation in post-stimulus EEG-fMRI responses was not predicted by the primary response amplitude. In the contralateral visual cortex we observed a decrease in both cerebral rate of oxygen metabolism (CMRO2) and CBF during the post-stimulus phase. In addition, the coupling ratio (n) between CMRO2 and CBF was significantly lower during the positive contralateral primary response phase compared with the post-stimulus phase and we propose that this reflects an altered balance of excitatory and inhibitory neuronal activity. Together our data provide strong evidence that the post-stimulus phase of the BOLD response has a neural origin which reflects, at least partially, an uncoupling of the neuronal responses driving the primary and post-stimulus responses, explaining the uncoupling of the signals measured in the two response phases. We suggest our results are consistent with inhibitory processes driving the post-stimulus EEG and fMRI responses. We therefore propose that new methods are required to model the post-stimulus and primary responses independently, enabling separate investigation of response phases in cognitive function and neurological disease.

Project description:Humans are rarely faced with one simple task, but are typically confronted with complex stimulus constellations and varying stimulus-relevance in a given situation. Through modifying the prototypical stop-signal task and by combined recording and analysis of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), we studied the effects of stimulus relevance for the generation of a response or its inhibition. Stimulus response mappings were modified by contextual cues, indicating which of two different stimuli following a go stimulus was relevant for stopping. Overall, response inhibition, that is comparing successful stopping to a stop-signal against go-signal related processes, was associated with increased activity in right inferior and left midfrontal regions, as well as increased EEG delta and theta power; however, stimulus-response conditions in which the most infrequent stop-signal was relevant for inhibition, were associated with decreased activity in regions typically involved in response inhibition, as well as decreased activity in the delta and theta bands as compared to conditions wherein the relevant stop-signal frequency was higher. Behaviorally, this (aforementioned) condition, which demanded inhibition only from the most infrequent stimulus, was also associated with reduced reaction times and lower error rates. This pattern of results does not align with typical stimulus frequency-driven findings and suggests interplay between task relevance and stimulus frequency of the stop-signal. Moreover, with a multimodal EEG-fMRI analysis, we demonstrated significant parameterization for response inhibition with delta, theta and beta time-frequency values, which may be interpreted as reflecting conflict monitoring, evaluative and/or motor processes as suggested by previous work (Huster et al., 2013; Aron, 2011). Further multimodal results suggest a possible neurophysiological and behavioral benefit under conditions whereby the most infrequent stimulus demanded inhibition, indicating that the frequency of the stop-signal interacts with the current stimulus-response contingency. These results demonstrate that response inhibition is prone to influence from other cognitive functions, making it difficult to dissociate real inhibitory capabilities from the influence of moderating mechanisms.

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Exploring the post-stimulus undershoot with spin-echo fMRI: implications for models of neurovascular response.

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Exploring the post-stimulus undershoot with spin-echo fMRI: implications for models of neurovascular response.

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