Evoked Neuronal Activity Accompanied by Transmitter Release Increases Oxygen Concentration in Rat Striatum in vivo but Not in vitro

Abstract

Dopamine and oxygen (O2) were measured in the caudate nucleus of anesthetized rats and in striatal slices during electrical stimulation. Simultaneous electrochemical detection of dopamine and O2 was accomplished with fast-scan cyclic voltammetry at a Nafion-coated carbon-fiber microelectrode. Stimulation of the medial forebrain bundle resulted in synaptic overflow of dopamine in the caudate nucleus. At the same time, O2 concentration increased in the extracellular fluid with two separate phases. The amplitude of the initial increase directly correlated with the frequency of the stimulus, with the time of maximum concentration reproducible across a range of frequencies. The second increase occurred at later times with a more random amplitude and with a broad, variable shape. Agents which blocked vasodilation affected both phases: atropine attenuated the initial increase, while the second feature was nearly absent after theophylline. Yohimbine and alpha-methyl-p-tyrosine did not affect the O2 responses. Local electrical stimulation of the slice preparation also resulted in dopamine overflow, but a prolonged decrease in O2 concentration accompanied this event. Striatal field stimulation in vivo produced changes in O2 concentration dependent on the relative position of the stimulating and working electrodes, but none of the responses resembled that seen in the caudate slice. Thus, while measurements in brain slices show O2 consumption as a result of stimulated neuronal activity, an apparent elevation of local cerebral blood flow during and after stimulation dominate the in vivo response.

Measurement of brain tissue oxygen at a carbon paste electrode can serve as an index of increases in regional cerebral blood flow

“…Assuming a maximum ECF concentration of 50 vmol/l, the above concentrations represent mean percentage increases of 889 15% and 5099% for tail pinch and grooming, respectively. Although O 2 utilisation increases during stimulated neuronal activity, the present results confirm previous findings that the rise in rCBF exceeds the increase in O 2 utilisation resulting in a net increase in O 2 (Leniger-Follert and Lü bbers, 1976;Fox et al, 1988;Zimmerman et al, 1992). For this reason O 2 currents provide an index of increases in rCBF only when such increases exceed O 2 utilisation.…”

“…Carbon electrodes are also more stable and in the case of CPEs have been found to be stable over several months in vivo (O'Neill and Fillenz, 1985). Recently, a new method for the measurement of dissolved O 2 in vivo involving Nafion™ modified carbon fibre disk electrodes (CFEs) and fast cyclic voltammetry has been reported by Wightman's group (Zimmerman and Wightman, 1991;Zimmerman et al, 1992). As a fastscan technique this method also has advantages associated with subsecond time resolution.…”

“…However, tissue concentration is determined by the balance between supply and utilisation. The use of a number of techniques has shown that during neuronal activation there is a rise in local O 2 concentration because of a greater increase in rCBF than O 2 utilisation (Leniger-Follert and Lü bbers, 1976;Fox et al, 1988;Zimmerman et al, 1992). We have previously reported the development of a voltammetric technique with subsecond time resolution for the direct measurement of tissue O 2 at a carbon paste electrode (Lowry et al, 1996).…”

Effects of Amphetamine and Evoked Dopamine Release on [11C]raclopride Binding in Anesthetized Cats

“…The stimulationinduced decreases in radioligand binding likely reflect changes in extracellular DA levels rather than alterations in cerebral blood flow (CBF). Simultaneous measurements of DA levels and oxygen consumption in the rat striatum have shown an elevation of local CBF during stimulation of the MFB in vivo (Zimmerman et al 1992). In another study, Chugani et al (1988) showed that CBF was not altered in the striatum following electrical nigrostriatal stimulations as measured with [ 14 C]iodoantipyrine.…”

Heterogeneous Dopamine Neurochemistry in the Striatum: The Fountain-Drain Matrix

“…at ASPET Journals on May 9, 2018 jpet.aspetjournals.org detected by carbon fiber electrodes and change in the striatum after MFB stimulation (Zimmerman and Wightman, 1991;Zimmerman et al, 1992;Cramer et al, 1997;Venton et al, 2003). DA oxidation and oxygen reduction occur at different potentials (ϩ0.3 and Ϫ1.4 V, respectively) (Zimmerman et al, 1992;Venton et al, 2003) and show a different kinetic response (Venton et al, 2003), ruling out the oxygen involvement on type II.…”