Cholinergic Modulation of Vibrissal Receptive Fields in Trigeminal Nuclei

Abstract

In sensory systems, it is usually considered that mesopontine cholinergic neurons exert their modulatory action in the thalamus by enhancing the relay of sensory messages during states of neural network desynchronization. Here, we report a projection heretofore unknown of these cholinergic cells to the interpolar division of the brainstem trigeminal complex in rats. After FluoroGold injection in the interpolar nucleus, a number of retrogradely labeled cells were found bilaterally in the pedunculopontine tegmental nucleus, and immunostaining revealed that the vast majority of these cells were also positive for choline acetyltransferase. Immunostaining for the acetylcholine vesicular transporter confirmed the presence of cholinergic terminals in the interpolar nucleus, where electron microscopy showed that they make symmetric and asymmetric synaptic contacts with dendrites and axon terminals. In agreement with these anatomical data, recordings in slices showed that the cholinergic agonist carbachol depolarizes large-sized interpolaris cells and increases their excitability. Local application of carbachol in vivo enhances responses to adjacent whiskers, whereas systemic administration of the cholinergic antagonist scopolamine produces an opposite effect. Together, these results show that mesopontine cholinergic neurons exert a direct, effective control over receptive field size at the very first relay stations of the vibrissal system in rodents. As far as receptive field synthesis in the lemniscal pathway relies on intersubnuclear projections from the spinal complex, it follows that cholinergic modulation of sensory transmission in the interpolar nucleus will have a direct bearing on the type of messages that is forwarded to the thalamus and cerebral cortex.

Angular Tuning Bias of Vibrissa-Responsive Cells in the Paralemniscal Pathway

“…Together, these factors provide a reasonable explanation for the gradients of response magnitude and onset latency observed in projection cells. They are also consistent with the observation that the receptive field size of projection cells depends strongly on a muscarinic modulation that produces a twofold increase in input resistance, so that scopolamine administration in vivo results in a marked shrinkage of receptive field size (Timofeeva et al, 2005); however, these factors alone do not explain why response magnitude depends on the direction of vibrissa displacement.…”

Excitatory neurons of the proprioceptive, interoceptive, and arousal hindbrain networks share a developmental requirement for Math1

“…Similarly, the CRH neurons of the BN connect with the RAS to stimulate arousal in response to interoceptive input (38,39). The NO/acetylcholine neurons of the RAS connect back to proprioceptive nuclei such as the spinal trigeminal nucleus in the medulla, where cholinergic stimulation increases the excitability of glutamatergic projection neurons (42). Some of these neurons then connect to the thalamus as part of conscious proprioception and others contribute to the cerebellar unconscious proprioceptive network (34).…”

Comprehensive mapping of whisker-evoked responses reveals broad, sharply tuned thalamocortical input to layer 4 of barrel cortex

“…It has been shown that some behavioral tasks require input from multiple whiskers (Krupa et al 2001), while others can be performed with only one intact whisker (Knutsen et al 2006). Inhibitory, neuromodulatory, and corticofugal projections have been shown to influence sensory stimulus encoding (Simons and Carvell 1989;Jacquin et al 1990;Lee et al 1994a, b;Fanselow and Nicolelis 1999;Castro-Alamancos 2002;Temereanca and Simons 2004;Timofeeva et al 2005;Higley and Contreras 2007;Li and Ebner 2007;Urbain and Deschenes 2007a,b;Furuta et al 2008;Lee et al 2008;Furuta et al 2010). All of these processes are potential contributors to this systemic flexibility.…”