Electrical stimulation of the mesencephalic ventral tegmental area evokes skeletal muscle vasodilatation in the cat and rat

Abstract

To test the hypothesis that the mesencephalic ventral tegmental area (VTA) plays a role in autonomic control of the cardiovascular system, we examined the cardiovascular effects of electrical stimulation of the mesencephalic ventral areas in anesthetized, paralyzed cats and rats. Electrical stimulation of the VTA for 30 s (100-μA current intensity; 40-50-Hz pulse frequency; 0.5-1-ms pulse duration) increased femoral blood flow by 130-162% in anesthetized cats and rats, whereas the identical stimulation of the substantial nigra (SN) failed to increase femoral blood flow. Electrical stimulation of the VTA also increased the arterial blood pressure and heart rate in anesthetized rats, but did not alter them in anesthetized cats. Accordingly, femoral vascular conductance was increased by 102-134% in both cats and rats. Atropine methyl nitrate (0.1 mg/kg) injected intravenously in the cats markedly attenuated the increases in femoral blood flow and vascular conductance. VTA stimulation was able to produce substantial increases in femoral blood flow and vascular conductance following a decerebration procedure performed at the premammillary and precollicular level in the cats, although their responses tended to attenuate to 55-69% of the control before the decerebration. Thus, it is likely that electrical stimulation of the VTA, but not the SN, is capable of evoking skeletal muscle vasodilatation, particularly via a sympathetically mediated cholinergic mechanism in the cat, and that the ascending projection from the VTA to the forebrain may not be responsible for the muscle vasodilatation.

Fig. 1

Typical recordings showing the effects of electrical stimulations of the mesencephalic ventral areas on arterial blood pressure, original and mean femoral blood flow, and femoral vascular conductance in an anesthetized, paralyzed cat. A The six sites of the stimulating electrode are shown in the frontal plane 3.0–3.5 mm anterior to the interaural line [14]. B Horizontal bars at the bottom indicate the 30-s period of electrical stimulation of each mesencephalic site. SC superior colliculus, CGN nucleus corporis geniculati medialis, PAG periaqueductal gray, RN red nucleus, SN substantia nigra, VTA ventral tegmental area, IPN nucleus interpeduncularis, cp cerebral peduncle

Fig. 2

Typical recordings showing the effects of electrical stimulations of the mesencephalic ventral areas on arterial blood pressure (AP), original and mean femoral blood flow, and femoral vascular conductance in an anesthetized, paralyzed rat. A The four sites of the stimulating electrode are shown in the frontal plane at the Bregma −5.30 to 5.60 [15]. B Horizontal bars at the bottom indicate the 30-s period of electrical stimulation of each mesencephalic site. A decrease in AP in B-a spontaneously appeared prior to electrical stimulation of the SN and was not related to the electrical stimulation. MGN medial genic nucleus, PAG periaqueductal gray, SNR substantia nigra pars reticulata, VTA ventral tegmental area, IPR interpeduncular nucleus, cp cerebral peduncle

Fig. 3

The changes in heart rate (HR), mean arterial blood pressure (MAP), and femoral blood flow and vascular conductance in response to electrical stimulations of the VTA and the SN are summarized in anesthetized cats and rats. Electrical stimulation of the VTA in cats (n = 8 cats) increased femoral blood flow and vascular conductance significantly (P < 0.05), while electrical stimulation of the VTA in rats (n = 4 rats) increased all of HR, MAP, and femoral blood flow and vascular conductance significantly (P < 0.05). In contrast to the VTA, electrical stimulation of the SN in the same cats and rats did not significantly (P > 0.05) increase any variables, except the HR in the rats. Asterisk indicates significant change from the baseline (P < 0.05). Dagger symbol indicates significant difference between the VTA and the SN (P < 0.05). NS not significantly different between the VTA and the SN (P > 0.05)

Fig. 4

The effects of atropine methyl nitrate (0.1 mg/kg) on the changes in HR, MAP, and femoral blood flow and vascular conductance evoked by electrical stimulation of the VTA (n = 6 cats). Atropine markedly blunted the increases in femoral blood flow and vascular conductance evoked by the VTA stimulation. Asterisk indicates significant difference (P < 0.05) before and after atropine. NS not significantly different (P > 0.05) before and after atropine

Fig. 5

The responses in HR, AP, and original and mean femoral blood flow evoked by electrical stimulation of the VTA before and after a decerebration procedure performed at the premammillary and precollicular level in an anesthetized, paralyzed cat. The substantial increase in femoral blood flow appeared during the VTA stimulation even following the decerebration procedure