Blood flow dynamics in different layers of the somatosensory region of the cerebral cortex on the rat during mechanical stimulation of the vibrissae

Abstract

The present work reports studies of the quantitative spatial and temporal characteristics of changes in local blood flow in different layers of the somatosensory cortex of rats during adequate mechanical stimulation of the vibrissae. Studies were performed using 34 Wistar rats. Skull trepanning was performed under urethane (1 g/kg) anesthesia. Television-guided microscopy was used to introduce a set of three platinum electrodes (100 microns in diameter, with tip diameters of 30-40 microns) into the somatosensory cortex projection zone of the vibrissae. The first and third electrodes were positioned in cortical layers I-III and IV-VI and the central electrode was used to generate hydrogen within the tissue. Electrode positions were confirmed histologically after experiments. Animals were placed on artificial ventilation and one or all vibrissae were stimulated at a frequency of 3 Hz for 60 sec, with interstimulus intervals of 3 min. Changes in the local blood flow were measured during stimulation and for 1 min afterwards, using the hydrogen clearance method, and brain tissue impedance was also measured. There was a small (up to 5-7%) reduction in blood flow in the first seconds of stimulation, which was followed 15-25 sec later by an increase and subsequent return to initial when stimulation stopped. The increases in blood flow during stimulation of all vibrissae were by 24.2 +/- 6.7% (n = 36) in layers IV-VI and 24.5 +/- 5.6% (n = 34) in layers I-III; increases in response to stimulation of single vibrissae were by 19.4 +/- 7.4% (n = 28) and 17.8 +/- 6.4% (n = 28) respectively. The dynamics of impedance changes corresponded to those of blood flow changes. Thus, heterogeneity was found in changes of local brain blood flow in different layers of the somatosensory cortex during increases in cortical functional activity.

Coupling and uncoupling of activity‐dependent increases of neuronal activity and blood flow in rat somatosensory cortex

“…The CBF increases were much smaller in the upper 0‐250 μm than in deeper cortical layers. This is consistent with results using mechanical whisker stimulation and the hydrogen clearance method (Moskalenko et al 1996, 1998), and a recent study using autoradiographic techniques (Gerrits et al 2000). The vascularity of the cortex may influence the flow signal as the highest capillary density is found in layer IV, corresponding to the maximal synaptic input (Patel, 1983).…”

High-Resolution fMRI Reveals Laminar Differences in Neurovascular Coupling between Positive and Negative BOLD Responses

“…It has been shown that hemodynamic regulation is heterogeneous and that functionally induced microvascular changes can occur at small spatial scales, i.e., at the level of columns and layers (Chaigneau et al, 2003; Erinjeri and Woolsey, 2002). Laminar differences in blood volume and flow have been observed in baseline conditions as well as after stimulation, showing that blood flow regulation differs between layers and between superficial vessels and parenchyma (Choi et al, 2010; Moskalenko et al, 1998; Zaharchuk et al, 1999). Baseline blood flow and vascularization are highest in the center of the cortex (Duvernoy et al, 1981; Gerrits et al, 2000; Moskalenko et al, 1998; Weber et al, 2008).…”

“…Laminar differences in blood volume and flow have been observed in baseline conditions as well as after stimulation, showing that blood flow regulation differs between layers and between superficial vessels and parenchyma (Choi et al, 2010; Moskalenko et al, 1998; Zaharchuk et al, 1999). Baseline blood flow and vascularization are highest in the center of the cortex (Duvernoy et al, 1981; Gerrits et al, 2000; Moskalenko et al, 1998; Weber et al, 2008). Upon stimulation, blood flow increases throughout the cortex, with the highest CBF increases in the middle layers (Moskalenko et al, 1998; Norup Nielsen and Lauritzen, 2001; Takano et al, 2006).…”

“…Baseline blood flow and vascularization are highest in the center of the cortex (Duvernoy et al, 1981; Gerrits et al, 2000; Moskalenko et al, 1998; Weber et al, 2008). Upon stimulation, blood flow increases throughout the cortex, with the highest CBF increases in the middle layers (Moskalenko et al, 1998; Norup Nielsen and Lauritzen, 2001; Takano et al, 2006). The BOLD, CBF, and CBV signals are a combination of the changes in the hemodynamic response and the signal characteristics of the fMRI methods: the BOLD signal is maximal at the cortical surface with a secondary peak in layer IV, reflecting the increased flow and oxygenation in the superficial veins and the middle layers; CBF and CBV peak in layer IV, reflecting the higher CBF and CBV in the center of the cortex and the sensitivity of these methods to microvessels, while the peak at the surface for CBV may reflect the increased CBV in superficial arteries and arterioles (Duong et al, 2000; Harel et al, 2006; Silva et al, 2000; Yu et al, 2012; Zappe et al, 2008; Zhao et al, 2006).…”

Apparent diffusion coefficient dependent fMRI: Spatiotemporal characteristics and implications on calibrated fMRI

“…We have proposed and demonstrated the use of dynamic ADC contrast to focus on the small vessel networks closely tied to the true neuronal activities (Ngai et al, 1995;Malonek and Grinvald, 1996;Moskalenko et al, 1998;Sheth et al, 2003), using multiple diffusion-weighting conditions. Diffusion-weighting selectively attenuates MR signals from proton pools undergoing a random-walk diffusion process (Torrey, 1956).…”