Total neuroenergetics support localized brain activity: Implications for the interpretation of fMRI

In α-chloralose-anesthetized rats, changes in the blood oxygenation level-dependent (BOLD) functional MRI (fMRI) signal (ΔS/S), and the relative spiking frequency of a neuronal ensemble (Δν/ν) were measured in the somatosensory cortex during forepaw stimulation from two different baselines. Changes in cerebral oxygen consumption (ΔCMR(O2)/CMR(O2)) were derived from the BOLD signal (at 7T) by independent determinations in cerebral blood flow (ΔCBF/CBF) and volume (ΔCBV/CBV). The spiking frequency was measured by extracellular recordings in layer 4. Changes in all three parameters (CMR(O2), ν, and S) were greater from the lower baseline (i.e., deeper anesthesia). For both baselines, ΔCMR(O2)/CMR(O2) and Δν/ν were approximately one order of magnitude larger than ΔS/S. The final values of CMR(O2) and ν reached during stimulation were approximately the same from both baselines. If only increments were required to support functions then their magnitudes should be independent of the baseline. In contrast, if particular magnitudes of activity were required, then sizes of increments should inversely correlate with the baseline (being larger from a lower baseline). The results show that particular magnitudes of activity support neural function. The disregard of baseline activity in fMRI experiments by differencing removes a large and necessary component of the total activity. Implications of these results for understanding brain function and fMRI experiments are discussed.

在α-氯醛糖（α-chloralose）麻醉的大鼠中，本研究设置两种不同基线条件，在前爪刺激过程中于躯体感觉皮层内检测了血氧水平依赖（BOLD）功能磁共振成像（fMRI）信号变化量（ΔS/S），以及神经元集群的相对放电频率变化量（Δν/ν）。脑氧代谢率（CMR(O2)）变化量（ΔCMR(O2)/CMR(O2)）则通过7T场强下的BOLD信号，结合独立测得的脑血流量（CBF）变化量（ΔCBF/CBF）与脑血容量（CBV）变化量（ΔCBV/CBV）推导得到。神经元放电频率通过皮层第四层的胞外记录进行测量。三种参数（CMR(O2)、ν与S）的变化量在较低基线条件下（即麻醉程度更深时）更为显著。在两种基线条件下，ΔCMR(O2)/CMR(O2)与Δν/ν的幅度均约为ΔS/S的一个数量级。刺激过程中CMR(O2)与ν所达到的最终稳态值，在两种基线条件下基本一致。若仅需通过活动增量来支撑神经功能，则增量幅度应与基线无关；与之相反，若神经活动需维持特定幅度，则增量幅度应与基线呈负相关（基线越低，增量越大）。本研究结果表明，神经功能依赖于特定幅度的活动水平。fMRI实验中通过差分法忽略基线活动，会移除总活动中占比可观且不可或缺的组成部分。本文最后讨论了上述结果对理解脑功能与fMRI实验的启示。