Physiological origin for the BOLD poststimulus undershoot in human brain: Vascular compliance versus oxygen metabolism

Russell H Morgan Department of Radiology and Radiological Science, Division of MR Research, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism (Impact Factor: 5.34). 04/2011; 31(7):1599-611. DOI: 10.1038/jcbfm.2011.35
Source: PubMed

ABSTRACT The poststimulus blood oxygenation level-dependent (BOLD) undershoot has been attributed to two main plausible origins: delayed vascular compliance based on delayed cerebral blood volume (CBV) recovery and a sustained increased oxygen metabolism after stimulus cessation. To investigate these contributions, multimodal functional magnetic resonance imaging was employed to monitor responses of BOLD, cerebral blood flow (CBF), total CBV, and arterial CBV (CBV(a)) in human visual cortex after brief breath hold and visual stimulation. In visual experiments, after stimulus cessation, CBV(a) was restored to baseline in 7.9±3.4 seconds, and CBF and CBV in 14.8±5.0 seconds and 16.1±5.8 seconds, respectively, all significantly faster than BOLD signal recovery after undershoot (28.1±5.5 seconds). During the BOLD undershoot, postarterial CBV (CBV(pa), capillaries and venules) was slightly elevated (2.4±1.8%), and cerebral metabolic rate of oxygen (CMRO(2)) was above baseline (10.6±7.4%). Following breath hold, however, CBF, CBV, CBV(a) and BOLD signals all returned to baseline in ∼20 seconds. No significant BOLD undershoot, and residual CBV(pa) dilation were observed, and CMRO(2) did not substantially differ from baseline. These data suggest that both delayed CBV(pa) recovery and enduring increased oxidative metabolism impact the BOLD undershoot. Using a biophysical model, their relative contributions were estimated to be 19.7±15.9% and 78.7±18.6%, respectively.

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Available from: Robert D. Stevens, Sep 04, 2015
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    • "The mechanism of the undershoot is debated, but likely a result of a sustained increase in high oxygen consumption after the stimulus has subsided (van Zijl et al., 2012). Vascular compliance also contributes to the undershoot (Hua et al., 2011; Zong and Huang, 2011) and may be important in our study since cocaine and amphetamine have known vasoactive properties (Chen et al., 2011; Gottschalk and Kosten, 2002). Recent work also suggests that the undershoot reflects inhibitory neural activity (Mullinger et al., 2013). "
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    • "CVR can be assessed by increasing the blood concentration of CO 2 , a potent vasodilator, while monitoring vascular responses using MRI. While MRI techniques to measure CBF and CBV changes have been utilized (Davis et al., 1998; Donahue et al., 2009a; Donahue et al., 2009b; Hoge et al., 1999; Hua et al., 2011; Mandell et al., 2008b), the BOLD sequence is by far the most widely used acquisition "
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    • "In the context of established biomechanical models such as the Balloon Model, a deep post-stimulus undershoot can be explained by an initially stiff post-capillary-bed venous compartment which becomes compliant after prolonged expansion , leading to the volume outflow of the system resembling a hysteresis loop (Buxton et al., 1998, 2004). Alternatively, there is also recent evidence to suggest that transient decoupling between the CBF and a sustained post-stimulus increase in the local cerebral metabolic rate of oxygen (CMRO 2 ) results in deoxygenated Hb accumulation and therefore a decrease in BOLD signal (Dechent et al., 2011; Hua et al., 2011). In the neonatal brain, the latter effect may predominate as marked increases in neuronal density and integration occur in the late preterm to term infant period, and these changes are associated with a significant maturational rise in CMRO 2 (Altman et al., 1988; Chugani and Phelps, 1986; Roche-Labarbe et al., 2011). "
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