Cholinergic modulation of non-N-methyl-d-aspartic acid glutamatergic transmission in the chick ventral lateral geniculate nucleus

Abstract

Neurotransmission between glutamatergic terminals of retinal ganglion cells and principal neurons of the ventral lateral geniculate nucleus (LGNv) was examined with patch clamp recordings in chick brain slices during electrical stimulation of the optic tract. Since muscarinic and nicotinic receptors are present in high densities in LGNv, the present study examined possible roles of both receptors in modulating retinogeniculate transmission. During whole-cell recordings from LGNv neurons, acetylcholine (ACh, 100 μM) caused an initial increase in amplitudes of optic tract-evoked non-NMDA glutamatergic postsynaptic currents (PSCs). This increase was unchanged when 1 μM atropine was present, indicating that this initial enhancement of PSCs was due entirely to activation of nicotinic receptors. However, during washout of ACh the amplitudes of evoked PSCs became significantly decreased by 40.4±5.0% for several minutes before recovering to their original amplitudes, an effect blocked by 1 μM atropine. Exogenously applied muscarine (10 μM) markedly depressed optic tract-evoked PSCs, and this decrease in amplitude was blocked by atropine. In a second set of experiments, we examined effects of releasing endogenous ACh prior to optic tract stimulation. This was accomplished by stimulation of the lateral portion of LGNv via a separate conditioning electrode. Following a brief train of low intensity conditioning stimuli, non-NMDA glutamatergic PSCs evoked by optic tract stimulation were potentiated. However, at higher conditioning stimulus intensities the PSCs were markedly decreased compared with control, and this decrease was partially blocked by atropine (1 μM). Neither ACh nor muscarine altered amplitudes of PSCs elicited by exogenously applied glutamate. Muscarine significantly reduced the frequency but not the amplitudes of miniature PSCs, consistent with a presynaptic location for muscarinic receptors mediating these effects. Thus while activation of nicotinic receptors potentiates retinogeniculate transmission, activation of muscarinic receptors mediates depression of transmission, demonstrating a complex cholinergic modulation of sensory information in LGNv.

Morphology, projection pattern, and neurochemical identity of Cajal's “centrifugal neurons”: The cells of origin of the tectoventrogeniculate pathway in pigeon (Columba livia) and chicken (Gallus gallus)

“…Retino-GLv terminals are known to be glutamatergic and, as the retino-tectal endings, endowed with nicotinic receptors (Guo et al, 1998(Guo et al, , 2005. Previous physiological work in chick brain slices has shown a nicotinic-dependent presynaptic enhancement of the synaptic transmission between the retinal terminals and the projection cells of the GLv-li (Guo et al, 2005(Guo et al, , 2010. Given their cholinergic character, vine-neurons are the most likely candidates to be the source of such modulation, since as we have shown here they end in the GLv-ne homotopically and in close apposition with the retinal terminals.…”

The Medial Ventrothalamic Circuitry: Cells Implicated in a Bimodal Network

“…In addition, retinal terminals in the GLv possess nicotinic receptors (Guo et al, 1998 , 2005 ), which may be modulated by tectal vine-neurons located in layer 10b (Vega-Zuniga et al, 2014 ). Interestingly, it has been shown that cholinergic modulation in the GLv can result in excitatory as well as inhibitory responses through nicotinic and muscarinic receptors (Guo and Chiappinelli, 2002 ; Guo et al, 2010 ). Also, GABAergic synapses are expected to occur due to the GABAergic neurochemical profile of GLv cells (Veenman and Reiner, 1994 ; Vega-Zuniga et al, 2016 ), and the presence of interneurons and projection neurons that have terminals either in the lamina interna (GLv-li) or neuropil (GLv-ne).…”

Muscarinic control of AMPA receptor responsiveness in mouse spinal cord motoneurons

“…Previous studies have established a potent muscarinic modulation of glutamatergic synaptic function at the presynaptic level in the striatum (Higley et al 2009), and in other central nervous regions (Li et al 2002; Guo et al 2010), including the lateral tegmental input onto hypoglossal motoneurons (Bellingham & Berger, 1996). Moreover, a form of EPSC depression induced by muscarinic receptors has been attributed to AMPA receptor internalization in the hippocampus (Volk et al 2007; Dickinson et al 2009).…”