The Microvascular System of the Striate and Extrastriate Visual Cortex of the Macaque

Max-Planck Institut für biologische Kybernetik, Spemannstr. 38, 72076 Tübingen, Germany.
Cerebral Cortex (Impact Factor: 8.67). 03/2008; 18(10):2318-30. DOI: 10.1093/cercor/bhm259
Source: PubMed


In functional neuroimaging, neurovascular coupling is used to generate maps of hemodynamic changes that are assumed to be surrogates of regional neural activation. The aim of this study was to characterize the microvascular system of the primate cortex as a basis for understanding the constraints imposed on a region's hemodynamic response by the vascular architecture, density, as well as area- and layer-specific variations. In the macaque visual cortex, an array of anatomical techniques has been applied, including corrosion casts, immunohistochemistry, and cytochrome oxidase (COX) staining. Detailed measurements of regional vascular length density, volume fraction, and surface density revealed a similar vascularization in different visual areas. Whereas the lower cortical layers showed a positive correlation between the vascular and cell density, this relationship was very weak in the upper layers. Synapse density values taken from the literature also displayed a very moderate correlation with the vascular density. However, the vascular density was strongly correlated with the steady-state metabolic demand as measured by COX activity. This observation suggests that although the number of neurons and synapses determines an upper bound on an area's integrative capacity, its vascularization reflects the neural activity of those subpopulations that represent a "default" mode of brain steady state.

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    • "However, Gardner's proposal for functional organization of the cortical vasculature is still tenable, if flow through penetrating arterioles is regulated by sphincters. We often observed focal constriction of the blood column in small pial branches (Fig. 4), as reported by others (Florey 1925; Rowbotham and Little 1962; Duvernoy et al. 1981; Harrison et al. 2002; Gordon et al. 2007; but see Weber et al. 2008). These putative sphincters appear to be innervated by the autonomic nervous system, potentially allowing neurogenic regulation of blood flow through individual penetrating arterioles (Baramidze et al. 1982, 1992). "
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    ABSTRACT: The vascular supply to layers and columns was compared in macaque primary visual cortex (V1) by labeling red blood cells via their endogenous peroxidase activity. Alternate sections were processed for cytochrome oxidase to reveal “patches” or “blobs,” which anchor the interdigitated column systems of striate cortex. More densely populated cell layers received the most profuse blood supply. In the superficial layers the blood supply was organized into microvascular lobules, consisting of a central venule surrounded by arterioles. Each vessel was identified as an arteriole or venule by matching it with the penetration site where it entered the cortex from a parent arteriole or venule in the pial circulation. Although microvascular lobules and cytochrome oxidase patches had a similar periodicity, they bore no mutual relationship. The size and density of penetrating arterioles and venules did not differ between patches and interpatches. The red blood cell labeling in patches and interpatches was equal. Moreover, patches and interpatches were supplied by an anastomotic pial arteriole system, with no segregation of blood supply to the two compartments. Often a focal constriction was present at the origin of pial arterial branches, indicating that local control of cortical perfusion may be accomplished by vascular sphincters.
    Cerebral Cortex 09/2014; DOI:10.1093/cercor/bhu221 · 8.67 Impact Factor
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    • "Thus, comparing task-related BOLD responses between areas and/or individuals is difficult to interpret [Ances et al., 2008; Buxton et al., 2004], given that regional variations in the brain venous network may predetermine the ability to detect reliable BOLD signals [Ekstrom, 2010] and thus explain the reason why certain brain areas are routinely found to be " activated " across a wide range of cognitive tasks [Gusnard and Raichle, 2001], whereas areas with an insufficient vascular network, that is low vascular density (VAD), may not produce functional response at all [Harrison et al., 2002]. This could be owing to the fact that areas with higher VAD reflect an increased signal-to-noise ratio of the BOLD signal and as a result increase the chances of detecting a difference between experimental conditions [Weber et al., 2008]. It is therefore important to fully characterize wholebrain venous vasculature prior to interpreting BOLD responses between brain areas and/or individuals. "
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    ABSTRACT: Functional magnetic resonance imaging (fMRI) has become one of the primary tools used for noninvasively measuring brain activity in humans. For the most part, the blood oxygen level-dependent (BOLD) contrast is used, which reflects the changes in hemodynamics associated with active brain tissue. The main advantage of the BOLD signal is that it is relatively easy to measure and thus is often used as a proxy for comparing brain function across population groups (i.e., control vs. patient). However, it is particularly weighted toward veins whose structural architecture is known to vary considerably across the brain. This makes it difficult to interpret whether differences in BOLD between cortical areas reflect true differences in neural activity or vascular structure. We therefore investigated how regional variations of vascular density (VAD) relate to the amplitude of resting-state and task-evoked BOLD signals. To address this issue, we first developed an automated method for segmenting veins in images acquired with susceptibility-weighted imaging, allowing us to visualize the venous vascular tree across the brain. In 19 healthy subjects, we then applied voxel-based morphometry (VBM) to T1-weighted images and computed regional measures of gray matter density (GMD). We found that, independent of spatial scale, regional variations in resting-state and task-evoked fMRI amplitudes were better correlated to VAD compared to GMD. Using a general linear model (GLM), it was observed that the bulk of regional variance in resting-state activity could be modeled by VAD. Cortical areas whose resting-state activity was most suppressed by VAD correction included Cuneus, Precuneus, Culmen, and BA 9, 10, and 47. Taken together, our results suggest that resting-state BOLD signals are significantly related to the underlying structure of the brain vascular system. Calibrating resting BOLD activity by venous structure may result in a more accurate interpretation of differences observed between cortical areas and/or individuals.
    Human Brain Mapping 05/2014; 35(5). DOI:10.1002/hbm.22301 · 5.97 Impact Factor
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    • "The narrowing of the cerebral vascular caliber in the capillary usually occurs at the sub-branches from the large blood vessels, while the narrowing of the cerebral vascular caliber in the penetrating vessels usually occurs at the inlet and the outlet. These results are similar to previous SEM results [25], [26], and these narrowing sites coincide with the distribution of the cerebral blood flow regulation sites. "
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    ABSTRACT: The topology of the cerebral vasculature, which is the energy transport corridor of the brain, can be used to study cerebral circulatory pathways. Limited by the restrictions of the vascular markers and imaging methods, studies on cerebral vascular structure now mainly focus on either observation of the macro vessels in a whole brain or imaging of the micro vessels in a small region. Simultaneous vascular studies of arteries, veins and capillaries have not been achieved in the whole brain of mammals. Here, we have combined the improved gelatin-Indian ink vessel perfusion process with Micro-Optical Sectioning Tomography for imaging the vessel network of an entire mouse brain. With 17 days of work, an integral dataset for the entire cerebral vessels was acquired. The voxel resolution is 0.35×0.4×2.0 µm(3) for the whole brain. Besides the observations of fine and complex vascular networks in the reconstructed slices and entire brain views, a representative continuous vascular tracking has been demonstrated in the deep thalamus. This study provided an effective method for studying the entire macro and micro vascular networks of mouse brain simultaneously.
    PLoS ONE 01/2014; 9(1):e88067. DOI:10.1371/journal.pone.0088067 · 3.23 Impact Factor
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