Differential organization of excitatory and inhibitory synapses within the rat dorsal vagal complex.
The dorsal motor nucleus of the vagus (DMV) is pivotal in the regulation of upper gastrointestinal functions, including motility and both gastric and pancreatic secretion. DMV neurons receive robust GABA- and glutamatergic inputs. Microinjection of the GABA(A) antagonist bicuculline (BIC) into the DMV increases pancreatic secretion and gastric motility, whereas the glutamatergic antagonist kynurenic acid (KYN) is ineffective unless preceded by microinjection of BIC. We used whole cell patch-clamp recordings with the aim of unveiling the brain stem neurocircuitry that uses tonic GABA- and glutamatergic synapses to control the activity of DMV neurons in a brain stem slice preparation. Perfusion with BIC altered the firing frequency of 71% of DMV neurons, increasing firing frequency in 80% of the responsive neurons and decreasing firing frequency in 20%. Addition of KYN to the perfusate either decreased (52%) or increased (25%) the firing frequency of BIC-sensitive neurons. When KYN was applied first, the firing rate was decreased in 43% and increased in 21% of the neurons; further perfusion with BIC had no additional effect in the majority of neurons. Our results indicate that there are several permutations in the arrangements of GABA- and glutamatergic inputs controlling the activity of DMV neurons. Our data support the concept of brain stem neuronal circuitry that may be wired in a finely tuned organ- or function-specific manner that permits precise and discrete modulation of the vagal motor output to the gastrointestinal tract.
Babic
Tanja
T
Department of Neural and Behavioral Sciences, Pennsylvania State College of Medicine, Hershey, Pennsylvania 17033, USA.
Browning
Kirsteen N
KN
Travagli
R Alberto
RA
D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D001933:Brain Stem / Q000187:drug effects / Q000502:physiology; D005260:Female; D018698:Glutamic Acid / Q000502:physiology; D007736:Kynurenic Acid / Q000494:pharmacology; D008297:Male; D008845:Microinjections; D009474:Neurons / Q000187:drug effects / Q000502:physiology; D018408:Patch-Clamp Techniques; D051381:Rats; D017207:Rats, Sprague-Dawley; D017552:Solitary Nucleus / Q000187:drug effects / Q000502:physiology*; D013569:Synapses / Q000502:physiology*; D014630:Vagus Nerve / Q000187:drug effects / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000502:physiology
D018698:Glutamic Acid; D005680:gamma-Aminobutyric Acid; D007736:Kynurenic Acid; D001640:Bicuculline