Localization of Activity-dependent Changes in Blood Volume to Submillimeter-scale Functional Domains in Cat Visual Cortex

Abstract

We have examined whether blood volume changes induced by neural activation are controlled precisely enough for us to visualize the submillimeter-scale functional structure in anesthetized and awake cat visual cortex. To activate the submillimeter-scale functional structures such as iso-orientation domains in the cortex, visual stimuli (gratings) were presented to the cats. Two methods were used to examine the spatial precision of blood volume changes including changes in total hemoglobin content and changes in plasma volume: (i) intrinsic signal imaging at the wavelength of hemoglobin's isosbestic point (569 nm) and (ii) imaging of absorption changes of an intravenously injected dye. Both measurements showed that the visual stimuli elicited stimulus-nonspecific and stimulus-specific blood volume changes in the cortex. The former was not spatially localized, while the latter was confined to iso-orientation domains. From the measurement of spatial separation of the iso-orientation domains, we estimated the spatial resolution of stimulus-specific blood volume changes to be as high as 0.6 mm. The changes in stimulus-nonspecific and -specific blood volume were not linearly correlated. These results suggest the existence of fine blood volume control mechanisms in the capillary bed in addition to global control mechanisms in arteries.

Mapping Iso-Orientation Columns by Contrast Agent-Enhanced Functional Magnetic Resonance Imaging: Reproducibility, Specificity, and Evaluation by Optical Imaging of Intrinsic Signal

“…However, our CBV-weighted fMRI and OIS data show that both plasma volume and RBC count increase within the same iso-orientation columns. Similar colocalization of activity-dependent changes in plasma volume and RBC count is also reported in studies comparing OIS imaging at the wavelength of the hemoglobin isosbestic points and optical imaging of intravascular plasma tracers in monkey ocular dominance column (Frostig et al, 1990), rodent barrel field (Narayan et al, 1995), and cat orientation column (Fukuda et al, 2005;Vanzetta et al, 2005). Combining our data with those of others, it can be concluded that the major mechanism of columnar-specific CBV response is not a redistribution of "RBC to plasma ratio" across cortical columns but rather dilation of microvessels within active columns.…”

“…Previously, neural correlates to OIS in visual cortex have only been demonstrated with dHb-weighted wavelengths (Grinvald et al, 1986;Shmuel and Grinvald, 1996;Maldonado et al, 1997;Bosking et al, 2002). However, good agreement between iso-orientation maps of 570 nm OIS and dHb-weighted OIS (Fukuda et al, 2005) (supplemental Fig. 2, available at www.jneurosci.org as supplemental material) suggests that 570 nm OIS is also a good neural correlate.…”

“…Because the ROI of the activation area contains singularities, our CNR may be underestimated. Intercolumnar distance in the isoorientation maps was determined within a 5 ϫ 5 mm activation area by autocorrelation analysis (Duong et al, 2001;Fukuda et al, 2005). To compare images obtained from different modalities, global subtraction was performed on all fMRI data to remove a slow signal fluctuation, and spatial filters (Table 1) were applied to remove spatial inhomogeneity.…”

Anesthesia and the Quantitative Evaluation of Neurovascular Coupling

“…Although the effects of focal excitation and surround inhibition on hemodynamic regulation are not fully understood (Boorman et al, 2010;Devor et al, 2007), the observed variation of the cortical mapping could depend on the actions of the anesthesia on both the neural and vascular components. Enhanced stimulus-specific localization of the cerebral blood volume (CBV)-weighted OIS (570 nm) under waking conditions relative to anesthetized conditions was observed for orientation column mapping in the cat visual cortex (Fukuda et al, 2005). Shtoyerman et al (2000) suggested that the increased specificity for the CBV response is due to an increased vascular response and signal transmission from neurons to vessels at the active columns because of the relatively unchanged spatial properties of neural responses.…”

Lessons from fMRI about Mapping Cortical Columns

“…7B; note that negative reflected 570-nm signal indicates an increase in CBV). This result implies that the preferred stimulation induces a smaller decrease in the dHb amount than the nonpreferred stimulation (i.e., less hyperoxygenation during the preferred stimulation) (Malonek and Grinvald, 1996;Grinvald et al, 2000;Fukuda et al, 2005). What causes this apparent contradiction of the supposed dHb signals between fMRI and optical imaging?…”