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. 2009 Aug;19(8):1776-86.
doi: 10.1093/cercor/bhn208. Epub 2008 Nov 21.

Differences in Response to Serotonergic Activation Between First and Higher Order Thalamic Nuclei

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Free PMC article

Differences in Response to Serotonergic Activation Between First and Higher Order Thalamic Nuclei

C Varela et al. Cereb Cortex. .
Free PMC article

Abstract

Two types of thalamic nuclei have been recognized: first order, which relay information from subcortical sources, and higher order, which may relay information from one cortical area to another. We have recently shown that muscarinic agonists depolarize all first order and most higher order relay cells but hyperpolarize a significant proportion of higher order relay cells. We now extend this result to serotonergic agonists, using rat thalamic brain slices and whole-cell, current- and voltage-clamp recordings from relay cells in various first order (the lateral geniculate nucleus, the ventral posterior nucleus, and the ventral portion of the medial geniculate body) and higher order nuclei (the lateral posterior, the posterior medial nucleus, and the dorsal portion of the medial geniculate body). Similar to the effects of muscarinic agonists, we found that first and most higher order relay cells were depolarized by serotonergic agonists, but 15% of higher order relay cells responded with hyperpolarization. Thus different subsets of higher order relay cells are hyperpolarized by these modulatory systems, which could have implications for the transfer of information between cortical areas.

Figures

Figure 1.
Figure 1.
(A) Schematic representation of thalamocortical driver connections (black arrows) and 2 brainstem modulatory thalamic afferents (colored arrows) for first order (FO) and higher order (HO) thalamic relays. Brainstem cholinergic (ACh) and serotonergic (5-HT) centers are schematically indicated. (B) Nissl stain of typical coronal slices used in our experiments. Top, slice including auditory thalamus with expanded: MGBd, dorsal portion of the medial geniculate body; MGBv, ventral portion of the medial geniculate body. Bottom, slice including visual and somatosensory thalamus with expanded inset: LGN, (dorsal) lateral geniculate nucleus; LP, lateral posterior nucleus; POm, posterior medial nucleus; VP, ventral posterior nucleus.
Figure 2.
Figure 2.
Effects of 5-HT on first and higher order relay cells. (A) Representative example of a first order relay cell's response to 5-HT (100 μM, ≈30 s). Downward deflections correspond to negative current pulses (−10 pA, 400 ms, 3–4 s between pulses) used to measure input resistance. Below the right part of the voltage trace is an inset showing the cell responses to steps of current injection, and similar insets are shown in (B)-(D). (B) Example representative of depolarizing responses observed in higher order relay cells. The upward spikes are truncated action potentials. The arrow here and in (C) indicates a period of adjustment of DC current injection. (C) Example representative of hyperpolarizing responses observed in higher order relay cells. (D) Example of a higher order cell showing a mixed response. (E) Dose–response curves for 5 cells, and they are labeled regarding nucleus of origin and response to 5-HT (DP, depolarizing; HP, hyperpolarizing). Abbreviations for nuclei as in Figure 1.
Figure 3.
Figure 3.
Population responses to 5-HT. (A) Frequency of the different effects of 5-HT on first and higher order relay cells. (B) Size of the depolarizing effect in first order and higher order nuclei. (C) Distribution of the effects in individual nuclei (first order in left column and higher order in right column). Abbreviations for nuclei as in Figure 1. Asterisks indicate significant difference.
Figure 4.
Figure 4.
Effect of 5-HT in older animals. (A) Current-clamp recording showing the effect of bath-applied 5-HT on a cell from the dorsal medial geniculate body of a 5-week-old rat. (B) Current-clamp recording of the effect of bath-applied 5-HT on a cell from the lateral posterior nucleus of a 7-week-old rat.
Figure 5.
Figure 5.
Effect of 5-HT on input resistance. (A, B) DC current injection during the peak of the effect was adjusted to bring the potential back to the baseline membrane potential to compare input resistance at the same voltage level. Expanded traces below each main trace show the negative current pulses (−10 pA, 400 ms; 3–4 s between pulses) used to measure input resistance. (C) Average input resistance (±SD) before, during and after the effect of 5-HT for first order depolarizing (left), higher order depolarizing (center), and higher order hyperpolarizing (right) cells. Asterisk indicates significant difference. (D) Input resistance before and during the effect of 5-HT effect for all the cells measured. Arrows locate examples shown in (A) and (B).
Figure 6.
Figure 6.
Direct postsynaptic effects of 5-HT. (A) Higher order relay cell depolarized by 5-HT in normal ACSF (left) is also depolarized by 5-HT in presence of low Ca2+ (0.5 mM)-high Mg2+ (8 mM) ACSF (right), which blocks synaptic transmission. (B) Effect on the response of a higher order relay cell hyperpolarized by 5-HT. (C) Population results for the low Ca2+-high Mg2+ experiments, showing the peak effect evoked by 5-HT before and in the presence of low Ca2+-high Mg2+ ACSF. Arrows locate examples shown in (A) and (B).
Figure 7.
Figure 7.
Effect of Methysergide (an antagonist for 5-HT1, 5-HT2, and 5-HT7 receptors) on 5-HT response. (A) Effect for a first order relay cell depolarized by 5-HT. (B) Voltage change caused by 5-HT before (control), during (+MS), and after (recovery) the application of methysergide (MS).

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