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The Journal of Neuroscience, April 12, 2006, 26(15):4015-4025; doi:10.1523/JNEUROSCI.5489-05.2006

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Behavioral/Systems/Cognitive
Cholinergic Modulation of Synaptic Transmission and Postsynaptic Excitability in the Rat Gracilis Dorsal Column Nucleus

David Fernández de Sevilla,¹ Margarita Rodrigo-Angulo,² Angel Nuñez,² and Washington Buño¹

¹Instituto Cajal, Consejo Superior de Investigaciones Científicas, 28002 Madrid, Spain, and ²Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, 28029 Madrid, Spain

Correspondence should be addressed to Dr. Angel Nuñez, Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, Arzobispo Morcillo 4, 28029 Madrid, Spain. Email: angel.nunez{at}uam.es

Somatosensory information, conveyed through the gracilis nucleus (GN), is regulated by descending corticofugal (CF) glutamatergic fibers. In addition, the GN receives cholinergic inputs with still unclear source and functional significance. Using both the in vitro slice and intracellular recording with sharp and patch electrodes and in vivo extracellular single-unit recordings, we analyzed the effects of activation of cholinergic receptors on synaptic, intrinsic, and functional properties of rat GN neurons. The cholinergic agonist carbamilcholine-chloride [carbachol (CCh); 1–10 µM] in vitro (1) induced presynaptic inhibition of EPSPs evoked by both dorsal column and CF stimulation, (2) increased postsynaptic excitability, and (3) amplified the spike output of GN neurons. The inhibition by atropine (1 µM) and pirenzepine (10 µM) of all presynaptic and postsynaptic effects of CCh suggests actions through muscarinic M₁ receptors. The above effects were insensitive to nicotinic antagonists. We searched the anatomical origin of the cholinergic projection to the GN throughout the hindbrain and forebrain, and we found that the cholinergic fibers originated mainly in the pontine reticular nucleus (PRN). Electrical stimulation of the PRN amplified sensory responses in the GN in vivo, an effect prevented by topical application of atropine. Our results demonstrate for the first time that cholinergic agonists induce both presynaptic and postsynaptic effects on GN neurons and suggest an important regulatory action of inputs from cholinergic neuronal groups in the pontine reticular formation in the functional control of somatosensory information flow in the GN.

Key words: gracile nuclei; cuneate nuclei; glutamatergic transmission; presynaptic inhibition; M₁ mAChR; somatosensory information; in vitro; in vivo

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Received Aug. 25, 2005; revised Feb. 17, 2006; accepted Feb. 17, 2006.

Correspondence should be addressed to Dr. Angel Nuñez, Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, Arzobispo Morcillo 4, 28029 Madrid, Spain. Email: angel.nunez{at}uam.es

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