Fine Detail of Neurovascular Coupling Revealed by Spatiotemporal Analysis of the Hemodynamic Response to Single Whisker Stimulation in Rat Barrel Cortex

Berwick, Jason; Johnston, Dave; Jones, Myles; Martindale, John; Martin, Chris; Kennerley, Aneurin J.; Redgrave, Peter; Mayhew, John E. W.

doi:10.1152/jn.00658.2007

Cited by 121 publications

(178 citation statements)

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“…Recent animal data have illustrated that longer duration stimulation may involve a separate later mechanism of neurovascular coupling, which induces a delayed more focal increase in CBV on the order of the capillary or pericyte. Berwick et al (2008) describe a late focal increase in CBV, which was not accompanied by an associated decrease in Hbr nor an increase in HbO 2 as in our study (Berwick et al, 2008). One possible explanation for persistent increases in hemoglobin oxygenation after triggered ADs would be the welldescribed postictal depolarization block (Dichter and Spencer, 1969).…”

Section: The Late Focal Overshoot In Epilepsysupporting

confidence: 55%

“…For example, cerebral blood volume (CBV) was originally thought to be poorly localized with neuronal activation, because the upstream arteriolar dilation spatially overperfuses the area of increased metabolic activity (Malonek and Grinvald, 1996). However, a careful analysis of the resulting optical signal revealed that a higher spatial correlation could be found at early time points, as CBV initially increases, and also at later time points during its dissolution, particularly with a long-duration stimulation (Berwick et al, 2008;Vanzetta et al, 2005). It is unknown whether a similar phenomenon exists during epileptiform activity and also whether animal data can be extrapolated to the human brain.…”

Section: Introductionmentioning

confidence: 99%

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The Importance of Latency in the Focality of Perfusion and Oxygenation Changes Associated with Triggered after Discharges in Human Cortex

Geneslaw

Zhao

et al. 2009

J Cereb Blood Flow Metab

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The spatiotemporal dynamics of neurovascular coupling during epilepsy are not well understood, and there are little data from studies of the human brain. We investigated changes in total hemoglobin (Hbt) and hemoglobin oxygenation in patients undergoing epilepsy surgery with intraoperative intrinsic optical spectroscopy (IOS) during triggered afterdischarges (ADs). We found an early (~0.5 secs) focal dip in hemoglobin oxygenation, arising precisely in the stimulated gyrus that lasted for 11.5 ± 10.0 secs, approximately the length of the AD (10.4 ± 4.4 secs). A later oxygen overshoot and increase in blood volume occurred in the adjacent surrounding gyri. After a significant delay (~20 to 30 secs), the overshoot and blood volume signal became extremely focal to the area of the onset of the AD. A smaller very late undershoot, the last phase of the ‘triphasic’ response, was also identified, although localization was inconsistent. In this study, we show that a ‘late focal overshoot’ and late Hbt signal may be extremely useful, in addition to the early dip, for the localization of seizure onset. It is likely that a separate mechanism underlies the persistent focal increase in cerebral blood volume after a long-duration cortical stimulation, compared with the nonspecific mechanism that causes the initial increase in cerebral blood flow.

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Section: The Late Focal Overshoot In Epilepsysupporting

confidence: 55%

Section: Introductionmentioning

confidence: 99%

The Importance of Latency in the Focality of Perfusion and Oxygenation Changes Associated with Triggered after Discharges in Human Cortex

Geneslaw

Zhao

et al. 2009

J Cereb Blood Flow Metab

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“…This gave an effective frame rate of 8 Hz for each wavelength and corresponding frequency estimates of hemodynamic changes. Spectral analysis was based upon the path length scaling algorithm (PLSA) described previously (Berwick et al, , 2008. Briefly, the algorithm used modified BeerLambert Law with a path length correction factor.…”

Section: Experiments 2: 2d-oismentioning

confidence: 99%

“…Briefly, the algorithm used modified BeerLambert Law with a path length correction factor. We estimated the concentration of hemoglobin in tissue at a concentration 104 M based on previous measurements (Kennerley et al, 2005) and saturation was calculated on a pixel by pixel basis (Berwick et al, 2008). The spectral analysis produced 2D images over time, of HbO 2 , Hbr, and total blood volume (Hbt).…”

Section: Experiments 2: 2d-oismentioning

confidence: 99%

Negative Blood Oxygen Level Dependence in the Rat:A Model for Investigating the Role of Suppression in Neurovascular Coupling

Boorman¹,

Kennerley²,

Johnston³

et al. 2010

J. Neurosci.

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150

144

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Modern neuroimaging techniques rely on neurovascular coupling to show regions of increased brain activation. However, little is known of the neurovascular coupling relationships that exist for inhibitory signals. To address this issue directly we developed a preparation to investigate the signal sources of one of these proposed inhibitory neurovascular signals, the negative blood oxygen level-dependent (BOLD) response (NBR), in rat somatosensory cortex. We found a reliable NBR measured in rat somatosensory cortex in response to unilateral electrical whisker stimulation, which was located in deeper cortical layers relative to the positive BOLD response. Separate optical measurements (two-dimensional optical imaging spectroscopy and laser Doppler flowmetry) revealed that the NBR was a result of decreased blood volume and flow and increased levels of deoxyhemoglobin. Neural activity in the NBR region, measured by multichannel electrodes, varied considerably as a function of cortical depth. There was a decrease in neuronal activity in deep cortical laminae. After cessation of whisker stimulation there was a large increase in neural activity above baseline. Both the decrease in neuronal activity and increase above baseline after stimulation cessation correlated well with the simultaneous measurement of blood flow suggesting that the NBR is related to decreases in neural activity in deep cortical layers. Interestingly, the magnitude of the neural decrease was largest in regions showing stimulus-evoked positive BOLD responses. Since a similar type of neural suppression in surround regions was associated with a negative BOLD signal, the increased levels of suppression in positive BOLD regions could importantly moderate the size of the observed BOLD response.

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“…In addition to this highly organized neuronal connectivity, the blood supply of each barrel is also functionally compartmentalized (Cox et al, 1993). Following vibrissae stimulation, brain imaging studies have visualized local increases in CBF in the barrels corresponding to the stimulated whiskers (Martin et al, 2002;Dunn et al, 2005;Berwick et al, 2008). Given the robustness of this paradigm, it has been used to identify several mediators of the evoked CBF response (for review, see Koehler et al, 2009;Cauli and Hamel, 2010).…”

Section: Introductionmentioning

confidence: 99%

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Lecrux

Toussay

Kocharyan

et al. 2011

Journal of Neuroscience

156

165

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The whisker-to-barrel cortex is widely used to study neurovascular coupling, but the cellular basis that underlies the perfusion changes is still largely unknown. Here, we identified neurons recruited by whisker stimulation in the rat somatosensory cortex using double immunohistochemistry for c-Fos and markers of glutamatergic and GABAergic neurons, and investigated in vivo their contribution along with that of astrocytes in the evoked perfusion response. Whisker stimulation elicited cerebral blood flow (CBF) increases concomitantly with c-Fos upregulation in pyramidal cells that coexpressed cyclooxygenase-2 (COX-2) and GABA interneurons that coexpressed vasoactive intestinal polypeptide and/or choline acetyltransferase, but not somatostatin or parvalbumin. The evoked CBF response was decreased by blockade of NMDA (MK-801, Ϫ37%), group I metabotropic glutamate (MPEPϩLY367385, Ϫ40%), and GABA-A (picrotoxin, Ϫ31%) receptors, but not by GABA-B, VIP, or muscarinic receptor antagonism. Picrotoxin decreased stimulus-induced somatosensory evoked potentials and CBF responses. Combined blockade of GABA-A and NMDA receptors yielded an additive decreasing effect (Ϫ61%) of the evoked CBF compared with each antagonist alone, demonstrating cooperation of both excitatory and inhibitory systems in the hyperemic response. Blockade of prostanoid synthesis by inhibiting COX-2 (indomethacin, NS-398), expressed by ϳ40% of pyramidal cells but not by astrocytes, impaired the CBF response (Ϫ50%). The hyperemic response was also reduced (Ϫ40%) after inhibition of astroglial oxidative metabolism or epoxyeicosatrienoic acids synthesis. These results demonstrate that changes in pyramidal cell activity, sculpted by specific types of inhibitory GABA interneurons, drive the CBF response to whisker stimulation and, further, that metabolically active astrocytes are also required.

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Fine Detail of Neurovascular Coupling Revealed by Spatiotemporal Analysis of the Hemodynamic Response to Single Whisker Stimulation in Rat Barrel Cortex

Abstract: Redgrave P, Mayhew JE. Fine detail of neurovascular coupling revealed by spatiotemporal analysis of the hemodynamic response to single whisker stimulation in rat barrel cortex.

Cited by 121 publications

References 50 publications

The Importance of Latency in the Focality of Perfusion and Oxygenation Changes Associated with Triggered after Discharges in Human Cortex

The Importance of Latency in the Focality of Perfusion and Oxygenation Changes Associated with Triggered after Discharges in Human Cortex

Negative Blood Oxygen Level Dependence in the Rat:A Model for Investigating the Role of Suppression in Neurovascular Coupling

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

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