Abstract
The relationship between changes in cerebral blood oxygenation and neuronal activity remains to be fully established. We compared somatosensory evoked potentials (SEP) and evoked cerebral blood oxygenation (CBO) changes in the sensorimotor cortex of the rat. In rats anesthetized with urethane and alpha-chloralose, we measured SEP and CBO using visible light spectroscopy (VLS) during neuronal activity. Increase of stimulus frequency caused a decrease of SEP amplitude, but an increase in concentration changes of deoxy-Hb and oxygen satu-ration. The difference in frequency responses between SEP and CBO might be caused by activation of inhibitory neurons, which could suppress excitatory neu-rons at high stimulus frequencies; activation of inhibitory neurons could reduce SEP amplitude, and increase oxygen saturation due to an increase of evoked cere-bral blood flow.
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Keywords
- Oxygen Saturation
- Sensorimotor Cortex
- Stimulus Frequency
- Inhibitory Neuron
- Somatosensory Evoke Potential
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1 Introduction
Increases in neuronal activity in the adult normal brain are accompanied by increases in regional cerebral blood flow (rCBF) that exceeds the changes in oxygen consumption, leading to a decrease in concentration of deoxyhemoglobin (deoxy-Hb) in the veins [1]. NIRS studies have revealed that neuronal activation generally causes a decrease of deoxy-Hb with increases of oxy-Hb and total-Hb in the activation cortical area of normal adults [2, 3]. However, the relationship between changes in cerebral blood oxygenation (CBO) and neuronal activity remains to be fully established. In the present study, we compared somatosensory evoked potentials (SEP) and evoked CBO changes in the sensorimotor cortex of the rat under various stimulus conditions.
2 Method
Male Fischer 344 rats (n = 7) weighing between 240 and 270 g were anesthetized with urethane (0.7 g/kg) and alpha-chloralose (0.06 g/kg). The right femoral artery was exposed and cannulated for the recording of arterial blood pressure and for sampling of blood gases. The right femoral vein was cannulated for drug administration. The rats were tracheotomized, paralyzed with pancuronium chloride (2 mg/kg/h), and mechanically ventilated with a mixture of air and oxygen to achieve physiological arterial blood levels of pH (7.33–7.50), PaO2 (150–210 mmHg), and PaCO2 (24–40 mmHg); arterial blood pressure had a range of 90–150 mmHg, and body temperature had a range of 36.2 to 36.8°C. The animals were secured in a stereotaxic frame.
The right parietal bone was thinned over the sensorimotor cortex. Bipolar needle electrodes were inserted beneath the skin in the contralateral forepaw, and the median nerve was stimulated for 10 s with pulses of 8.0 mA intensity and 100 μs duration, at frequencies between 1 and 50 Hz. We recorded SEP and VLS positioned on the forepaw projection area of the somatosensory cortex. We measured SEP amplitude (P1 + N1 amplitude), and calculated ΣSEP amplitude (=SEP amplitude × stimulus frequency) [4].
We evaluated evoked CBO changes in the sensorimotor cortex using visible light spectroscopy (VLS) (C-9183, Hamamatsu Photonics, Japan) during median nerve stimulation with the same stimulus conditions as for SEP. VLS measures the changes of oxy-Hb and deoxy-Hb concentrations in the cerebral vessels based on the characteristic absorption spectra of hemoglobin in the visible light range [5]. White light from the LED was directed at the tissue through a fiber optic bundle, and reflected light was transmitted to a cooled charge-coupled-device spectrome-ter. The relative concentration changes of oxy-Hb and deoxy-Hb were calculated by least-squares error curve-fitting based on the differential spectrum: the ana-lyzed wavelength range was 520–580 nm. The VLS parameters were oxy-Hb, de-oxy-Hb, total-Hb (=oxy-Hb+deoxy-Hb) and oxygen saturation; total-Hb reflects cerebral blood volume (CBV). The sampling rate was 0.5 s.
The data were expressed as means ± SD. Statistical significance of differences was determined by analysis of variance (ANOVA) followed by Dunnet’s test, us-ing StatView (Abacus Concepts, USA). P values less than 0.05 were considered as indicating statistical significance.
3 Results
The evoked CBO changes appeared approximately 1.5 s after the stimulus onset. We observed increases of oxy-Hb and oxygen saturation associated with a decrease of deoxy-Hb during activation. Fig. 1a,b, showed examples of changes in oxygen saturation and deoxy-Hb caused by rat forepaw stimuli using VLS. Increases of stimulus frequency caused increases of oxy-Hb and oxygen saturation associated with a decrease of deoxy-Hb; however, total-Hb did not change with increase of the stimulus frequency. The CBO change reached maximum at 50 Hz. There were significant differences in oxygen saturation and deoxy-Hb between 1 and 50 Hz (p < 0.05) (Fig. 1c,d).
The SEP amplitude declined with increase of the stimulus frequency (Fig. 2a). In contrast to evoked CBO changes, the maximum ∑SEP amplitude was observed at 2 Hz (Fig. 2b).
4 Discussion
We observed that an increase of stimulus frequency caused increases of oxy-Hb and oxygen saturation with a concomitant decrease of deoxy-Hb. This CBO change is consistent with the evoked CBO change observed during a focal increase of neuronal activity [2, 3]. Positron emission tomography demonstrated that increases of neuronal activity are accompanied by increases of rCBF that exceed the changes in oxygen consumption, leading to a decrease of deoxy-Hb in the veins [1].
Increase of stimulus frequency caused an increase of oxygen saturation with a decrease of deoxy-Hb, which reached the maximum levels at 50 Hz. In contrast, the maximum ∑SEP amplitude was observed at 5 Hz. Ngai et al., employing the same equation for ∑SEP amplitude, evaluated the frequency response of ∑SEP amplitude (1˜20 Hz), and observed the maximum ∑SEP amplitude at 5 Hz [4]. While it is possible that the reductions of SEP are due to either inhibitory mechanisms, habituation of the peripheral nerve, or limitations of transmission of the sensory input, several studies have suggested that inhibitory mechanisms play the most important role in the reduction of SEP at high stimulus frequency [6, 7]. This might explain the physiological mechanism of the difference in frequency responses between SEP and evoked CBO responses. That is, activation of inhibitory neurons at high stimulus frequencies causes an increase of neuronal oxidative metabolism, resulting in an increase of CBO response at high stimulus frequencies. Indeed, Igarashi et al. evaluated the frequency response of the evoked changes in autofluorescence of flavoproteins, which reflect neuronal oxidative metabolism, and observed that the fluorescence attained maximal intensity at 50 Hz [8].
5 Conclusion
We compared SEP and evoked CBO changes in the sensorimotor cortex of the rat. Increases of stimulus frequency caused a decrease of SEP amplitude, but an increase of oxygen saturation with a decrease of deoxy-Hb; however, changes of stimulus frequency did not affect total-Hb concentration. Activation of inhibitory neurons at high stimulus frequencies could decrease the SEP amplitude, but in-crease evoked CBO changes.
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Kondo, Y. et al. (2010). Comparison of Somatosensory Evoked Potentials and Cerebral Blood Oxygenation Changes in the Sensorimotor Cortex During Activation in the Rat. In: Takahashi, E., Bruley, D. (eds) Oxygen Transport to Tissue XXXI. Advances in Experimental Medicine and Biology, vol 662. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-1241-1_35
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DOI: https://doi.org/10.1007/978-1-4419-1241-1_35
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