Modulatory effects of acetylcholine, serotonin and noradrenaline on the activity of cat perigeniculate neurons.
We studied the modulatory actions of microiontophoretically applied acetylcholine (ACH), serotonin (5-HT, 5-hydroxytryptamine) and noradrenaline (NA), and those of the adrenoceptor agonists phenylephrine (PHE, alpha 1), clonidine (CLO, alpha 2) and isoprenaline (ISO, beta) on spontaneous and visually induced activities in cat perigeniculate (PGN) and thalamic reticular (NRT) neurons (only spontaneous) during extracellular recordings performed in vivo. ACH and 5-HT were found to affect the ongoing (spontaneous) and visually evoked activity of PGN cells and also the spontaneous activity of NRT cells in an opposite fashion. ACH inhibited tonic firing and often induced burst activity. By contrast, 5-HT exerted an excitatory influence, which caused a long-lasting, very regular, high-frequency activity between about 35 and 120 Hz. Spontaneous as well as 5-HT-induced firing was found to prefer three distinct frequency ranges: 35-42 Hz, 60-67 Hz and 80-120 Hz. Opposite actions of ACH and 5-HT were also evident when applied simultaneously. ACH dampened the high-frequency activity elicited with 5-HT, and 5-HT could replace the burst activity induced with ACH application by a regular tonic activity. The absolute strength of visual responses (in spikes per second) was only slightly enhanced or reduced by ACH and 5-HT, respectively, but due to the strong effects on background activity, ACH clearly elevated the signal-to-noise ratio and 5-HT reduced it. Despite its excitatory action, 5-HT did not facilitate visual responses. Spontaneous changes in ongoing activity were found to affect the visual response amplitude in the same way. Noradrenaline, the alpha 1-agonist PHE and the beta-agonist ISO exerted a weak depressant action on high-frequency maintained activity, but during low-frequency single spike activity and/or burst activity a facilitatory effect was evident, which prevented the generation of burst discharges and slightly increased single spike firing. Visually evoked activity was little affected, but signal-to-noise ratio changed with changes in ongoing activity. The alpha 2-agonist CLO clearly attenuated both spontaneous activity and visual responses. We suggest that, in addition to direct effects of ACH and 5-HT on geniculate relay cells, the balance between the opposite actions of ACH and 5-HT on PGN cells determines the mode of operation in the recurrent inhibitory circuit: either a global, tonic inhibition of relay cells during a dominating 5-HT influence or a less tonic but phasic inhibition during increased activity in the cholinergic system.
Funke
K
K
Abteilung für Neurophysiologie, Medizinische Fakultät, Ruhr-Universität, Bochum, Germany.
Eysel
U T
UT
D000109:Acetylcholine / Q000494:pharmacology*; D000818:Animals; D002415:Cats; D005074:Evoked Potentials, Visual / Q000187:drug effects; D005260:Female; D005829:Geniculate Bodies / Q000166:cytology / Q000187:drug effects*; D007478:Iontophoresis; D008297:Male; D009474:Neurons / Q000187:drug effects*; D009638:Norepinephrine / Q000494:pharmacology*; D010775:Photic Stimulation; D012701:Serotonin / Q000494:pharmacology*; D013564:Sympathetic Nervous System / Q000187:drug effects; D013787:Thalamic Nuclei / Q000166:cytology / Q000187:drug effects
D012701:Serotonin; D000109:Acetylcholine; D009638:Norepinephrine