Contribution of Excitatory and Inhibitory Neuronal Activity to BOLD fMRI

Moon, Hyun Seok; Jiang, Haiyan; Vo, Thanh Tan; Jung, Won Beom; Vazquez, Alberto L.; Kim, Seong‐Gi

doi:10.1093/cercor/bhab068

Cited by 52 publications

(40 citation statements)

References 50 publications

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“…1 E ). Since inhibitory neural activation induces a hemodynamic response at the stimulation site ( 36 , 37 ) and in downstream regions, the contribution by this type of activation should be removed. It is assumed that the common photostimulation-driven hemodynamic response is completely eliminated by calculating the difference between the optogenetic fMRI responses observed with and without sensory stimulation (Comb − Opto = Diff in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Although GABAergic interneuron activity is known to regulate local vascular tone by the release of vasoactive mediators (e.g., nitric oxide) ( 49 ), their activity also interacts with nearby excitatory neurons in the cortex. When inhibitory neurons were activated in VGAT-ChR2 mice, an increase in CBF and CBV was observed for <5 s of stimulation ( 37 , 50 , 51 ), indicating that inhibitory neurons indeed increase hemodynamic responses. However, the increased inhibitory activity by optogenetic stimulation suppressed excitatory activity (inhibition), which led to a decrease in hemodynamic responses.…”

Section: Discussionmentioning

confidence: 96%

“…Therefore, hemodynamic responses may be closely dependent on stimulus frequency and duration. Notably, we recently investigated the contribution of inhibitory neuronal activity to fMRI responses using multimodal measurements with electrophysiology, BOLD fMRI, and optical-imaging during ChR2 stimulation of inhibitory neurons in VGAT-ChR2 mice ( 37 ). Under the same stimulation parameters, biphasic BOLD fMRI and CBV-weighted optical-imaging responses were observed at the stimulated site with increased inhibitory and decreased excitatory neuronal activity; an initial small positive change (by increased inhibitory activity) was followed by a prolonged negative response (by suppressed excitatory activity).…”

Section: Discussionmentioning

confidence: 99%

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Dissection of brain-wide resting-state and functional somatosensory circuits by fMRI with optogenetic silencing

Jung

Jiang

Lee³

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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To further advance functional MRI (fMRI)–based brain science, it is critical to dissect fMRI activity at the circuit level. To achieve this goal, we combined brain-wide fMRI with neuronal silencing in well-defined regions. Since focal inactivation suppresses excitatory output to downstream pathways, intact input and suppressed output circuits can be separated. Highly specific cerebral blood volume–weighted fMRI was performed with optogenetic stimulation of local GABAergic neurons in mouse somatosensory regions. Brain-wide spontaneous somatosensory networks were found mostly in ipsilateral cortical and subcortical areas, which differed from the bilateral homotopic connections commonly observed in resting-state fMRI data. The evoked fMRI responses to somatosensory stimulation in regions of the somatosensory network were successfully dissected, allowing the relative contributions of spinothalamic (ST), thalamocortical (TC), corticothalamic (CT), corticocortical (CC) inputs, and local intracortical circuits to be determined. The ventral posterior thalamic nucleus receives ST inputs, while the posterior medial thalamic nucleus receives CT inputs from the primary somatosensory cortex (S1) with TC inputs. The secondary somatosensory cortex (S2) receives mostly direct CC inputs from S1 and a few TC inputs from the ventral posterolateral nucleus. The TC and CC input layers in cortical regions were identified by laminar-specific fMRI responses with a full width at half maximum of <150 µm. Long-range synaptic inputs in cortical areas were amplified approximately twofold by local intracortical circuits, which is consistent with electrophysiological recordings. Overall, whole-brain fMRI with optogenetic inactivation revealed brain-wide, population-based, long-range circuits, which could complement data typically collected in conventional microscopic functional circuit studies.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Dissection of brain-wide resting-state and functional somatosensory circuits by fMRI with optogenetic silencing

Jung

Jiang

Lee³

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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“…Since MRI studies rely on Blood Oxygen Level Dependent (BOLD) signals as surrogates for neuronal activity (Hillman, 2014;Howarth et al, 2021;Moon et al, 2021), it is possible that changes in rCBF reflect changes in underlying neuronal activity. For instance, cerebral cortex hypoperfusion in ASD patients could reflect lower metabolic demands (Schifter et al, 1994).…”

Section: Altered Cerebral Blood Flow In Autism Spectrum Disordersmentioning

confidence: 99%

From Neurodevelopmental to Neurodegenerative Disorders: The Vascular Continuum

Ouellette

Lacoste

2021

Front. Aging Neurosci.

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Structural and functional integrity of the cerebral vasculature ensures proper brain development and function, as well as healthy aging. The inability of the brain to store energy makes it exceptionally dependent on an adequate supply of oxygen and nutrients from the blood stream for matching colossal demands of neural and glial cells. Key vascular features including a dense vasculature, a tightly controlled environment, and the regulation of cerebral blood flow (CBF) all take part in brain health throughout life. As such, healthy brain development and aging are both ensured by the anatomical and functional interaction between the vascular and nervous systems that are established during brain development and maintained throughout the lifespan. During critical periods of brain development, vascular networks remodel until they can actively respond to increases in neural activity through neurovascular coupling, which makes the brain particularly vulnerable to neurovascular alterations. The brain vasculature has been strongly associated with the onset and/or progression of conditions associated with aging, and more recently with neurodevelopmental disorders. Our understanding of cerebrovascular contributions to neurological disorders is rapidly evolving, and increasing evidence shows that deficits in angiogenesis, CBF and the blood-brain barrier (BBB) are causally linked to cognitive impairment. Moreover, it is of utmost curiosity that although neurodevelopmental and neurodegenerative disorders express different clinical features at different stages of life, they share similar vascular abnormalities. In this review, we present an overview of vascular dysfunctions associated with neurodevelopmental (autism spectrum disorders, schizophrenia, Down Syndrome) and neurodegenerative (multiple sclerosis, Huntington’s, Parkinson’s, and Alzheimer’s diseases) disorders, with a focus on impairments in angiogenesis, CBF and the BBB. Finally, we discuss the impact of early vascular impairments on the expression of neurodegenerative diseases.

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“…The physiological mechanisms underlying the task-induced negative BOLD phenomenon (deactivation) remain unclear [28], which is thought to be dependent on the stimulus type (task) and brain region [29]. However, numerous recent studies have suggested that this phenomenon may reflect neuronal inhibition [30][31][32][33][34][35][36][37][38] without exception in the central sensory-motor network [39,40].…”

Section: Negative Bold Phenomenonmentioning

confidence: 99%

Existence of Interhemispheric Inhibition between Foot Sections of Human Primary Motor Cortices: Evidence from Negative Blood Oxygenation-Level Dependent Signal

et al. 2021

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Interhemispheric inhibition (IHI) between the left and right primary motor cortices (M1) plays an important role when people perform an isolated unilateral limb movement. Moreover, negative blood oxygenation-level dependent signal (deactivation) obtained from the M1 ipsilateral to the limb could be a surrogate IHI marker. Studies have reported deactivation in the hand section of the ipsilateral M1 during simple unilateral hand movement. However, deactivation in the foot section during unilateral foot movement has not been reported. Therefore, IHI between the foot sections of the bilateral M1s has been considered very weak or absent. Thirty-seven healthy adults performed active control of the right foot and also passively received vibration to the tendon of the tibialis anterior muscle of the right foot, which activates the foot section of the contralateral M1, with brain activity being examined through functional magnetic resonance imaging. The vibration and active tasks significantly and non-significantly, respectively, deactivated the foot section of the ipsilateral M1, with a corresponding 86% and 60% of the participants showing decreased activity. Thus, there could be IHI between the foot sections of the bilateral M1s. Further, our findings demonstrate between-task differences and similarities in cross-somatotopic deactivation.

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Contribution of Excitatory and Inhibitory Neuronal Activity to BOLD fMRI

Cited by 52 publications

References 50 publications

Dissection of brain-wide resting-state and functional somatosensory circuits by fMRI with optogenetic silencing

Dissection of brain-wide resting-state and functional somatosensory circuits by fMRI with optogenetic silencing

From Neurodevelopmental to Neurodegenerative Disorders: The Vascular Continuum

Existence of Interhemispheric Inhibition between Foot Sections of Human Primary Motor Cortices: Evidence from Negative Blood Oxygenation-Level Dependent Signal

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