Oxygen consumption by spiking activity in rat cerebellum

Introduction

The mechanisms coupling neuronal activity, cerebral metabolism and cerebral blood flow (CBF) during activation as well as in the basal state (rest) are not clear. The type of neuronal activity, i.e., synaptic input or action potential output (spiking activity), responsible for energy consumption is under debate. We here examined the effect of basal spiking activity per se on oxygen consumption in the cerebllar cortex in rats.

Methods

Spiking activity, as well as field potentials, and tissue oxygen tension (tpO2) were measured at the same cortical depth using glass microelectrodes (tip diameter 2 mm) and Clark-type oxygen electrodes (tip diameter 3–4 μm), respectively. CBF was recorded with laser-Doppler flowmetry. All experiments were carried out using an open cranial window preparation placed over the cerebellar vermis in a-chloralose-anaesthetized adult male Wistar rats (n = 6). Basal measurements were performed in control conditions and after superfusion of the cerebellum with the GABAA antagonist, bicuculline (0.2 mM). Parallel fiber stimulation with 30 s stimulation trains at 0.5, 5, 10, and 15 Hz was given before and after bicuculline application.

Results

As we have shown previously, application of bicuculline caused basal spiking activity to increase 3–4 fold without influencing either basal CBF or mean arterial blood pressure. Maximal effect of bicuculline on spike rate was achieved after 3–12 minutes of exposure to the GABAA antagonist. PO2 was measured directly before bicuculline application and when maximal spike rate occurred. In 5 of 6 rats, pO2 decreased, while remaining unchanged in the sixth. Averaging results from all rats, pO2 decreased by 25% at maximal spike rate and this decrease was maintained during the 30 minute observation period. In the parallel fiber system, the magnitude of field potential amplitude, representing synaptic input, appeared to increase in the presence of bicuculline (control: 0.082 mV vs bicuculline: 0.116 mV) without reaching significance (p = 0.1522).

Conclusion

We conclude that basal spiking activity per se increases cerebellar oxidative metabolism. We have previously shown that synaptic input via the climbing fibers is not influenced by GABAA antagonism. In the parallel fiber system, however, increased synaptic input via the parallel fibers may be a contributing factor to both spiking activity and brain metabolism.