A novel central pathway links arterial baroreceptors and pontine parasympathetic neurons in cerebrovascular control

• Published in: Cellular and molecular neurobiology 2003-10, Vol.23 (4-5), p.463-478
• Main Authors: Agassandian, Khristofor, Fazan, Valeria P S, Margaryan, Naira, Dragon, Deidre Nitschke, Riley, Jeffrey, Talman, William T
• Format: Article
• Language: English
• Subjects: Animals; Autonomic Pathways - drug effects; Autonomic Pathways - physiology; Autonomic Pathways - ultrastructure; Baroreceptors; Baroreflex - drug effects; Baroreflex - physiology; Blood flow; Blood pressure; Blood Pressure - drug effects; Blood Pressure - physiology; Cardiovascular system; Cerebral Arteries - innervation; Cerebral Arteries - physiology; Cerebral blood flow; Cerebrovascular Circulation - drug effects; Cerebrovascular Circulation - physiology; Denervation; Ganglia; Ganglia, Parasympathetic - drug effects; Ganglia, Parasympathetic - physiology; Ganglia, Parasympathetic - ultrastructure; Glutamic Acid - metabolism; Glutamic Acid - pharmacology; Male; Microscopy, Electron; Nitric oxide; Nitric Oxide - biosynthesis; Nitric Oxide Synthase - antagonists & inhibitors; Nitric Oxide Synthase - metabolism; Parasympathetic nervous system; Parasympathetic Nervous System - drug effects; Parasympathetic Nervous System - physiology; Parasympathetic Nervous System - ultrastructure; Pons; Pons - drug effects; Pons - physiology; Pons - ultrastructure; Pressoreceptors - physiology; Pressoreceptors - ultrastructure; Presynaptic Terminals - drug effects; Presynaptic Terminals - metabolism; Presynaptic Terminals - ultrastructure; Pterygopalatine ganglion; Rats; Rats, Sprague-Dawley; Solitary Nucleus - physiology; Solitary Nucleus - ultrastructure; Solitary tract nucleus; Vasodilation
• ISSN: 0272-4340; 1573-6830
• DOI: 10.1023/A:1025059710382

1. We tested the hypothesis that arterial baroreceptor reflexes modulate cerebrovascular tone through a pathway that connects the cardiovascular nucleus tractus solitarii with parasympathetic preganglionic neurons in the pons. 2. Anesthetized rats were used in all studies. Laser flowmetry was used to measure cerebral blood flow. We assessed cerebrovascular responses to increases in arterial blood pressure in animals with lesions of baroreceptor nerves, the nucleus tractus solitarii itself, the pontine preganglionic parasympathetic neurons, or the parasympathetic ganglionic nerves to the cerebral vessels. Similar assessments were made in animals after blockade of synthesis of nitric oxide, which is released by the parasympathetic nerves from the pterygopalatine ganglia. Finally the effects on cerebral blood flow of glutamate stimulation of pontine preganglionic parasympathetic neurons were evaluated. 3. We found that lesions at any one of the sites in the putative pathway or interruption of nitric oxide synthesis led to prolongation of autoregulation as mean arterial pressure was increased to levels as high as 200 mmHg. Conversely, stimulation of pontine parasympathetic preganglionic neurons led to cerebral vasodilatation. The second series of studies utilized classic anatomical tracing methods to determine at the light and electron microscopic level whether neurons in the cardiovascular nucleus tractus solitarii, the site of termination of baroreceptor afferents, projected to the pontine preganglionic neurons. Fibers were traced with anterograde tracer from the nucleus tractus solitarii to the pons and with retrograde tracer from the pons to the nucleus tractus solitarii. Using double labeling techniques we further studied synapses made between labeled projections from the nucleus tractus solitarii and preganglionic neurons that were themselves labeled with retrograde tracer placed into the pterygopalatine ganglion. 4. These anatomical studies showed that the nucleus tractus solitarii directly projects to pontine preganglionic neurons and makes asymmetric, seemingly excitatory, synapses with those neurons. These studies provide strong evidence that arterial baroreceptors may modulate cerebral blood flow through direct connections with pontine parasympathetic neurons. Further study is needed to clarify the role this pathway plays in integrative physiology.