Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat

Hyung-Il Lee; Soo-Joung Park

doi:10.5395/JKACD.2002.27.6.587

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Original Article Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat: Hyung-Il Lee, Soo-Joung Park^*; Journal of Korean Academy of Conservative Dentistry 2002;27(6):587-599.
DOI: https://doi.org/10.5395/JKACD.2002.27.6.587
Published online: November 30, 2002

Department of Conservative Dentistry, College of Dentistry, Chonbuk National University, Korea.

^*Department of Oral Physiology and Institute of Oral Bioscience, College of Dentistry, Chonbuk National University, Korea.

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Abstract
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Abstract

Extracellular single unit recordings were made from the ventral posteromedial thalamic (VPM) nociceptive neurons to determine mechanoreceptive field (RF) and response properties. A total of 44 VPM thalamic nociceptive neurons were isolated from rats anesthetized with urethane-chloralose.

Based on responses to various mechanical stimuli including touch, pressure and pinch applied to the RF, 32 of 44 neurons were classified as nociceptive specific (NS) neuron. The other 12 neurons, classified as wide dynamic range (WDR), showed a graded response to increasingly intense stimuli, with a maximum discharge to noxious pinch.

The VPM nociceptive neurons showed various spontaneous activity ranged from 0-6 Hz. They were located throughout the VPM, and had an contralateral RF including mainly intraoral (and perioral) regions. The RF size was relatively small, and very few neurons had a receptive field involving 3 trigeminal divisions. The NS neurons activated only by pressure and pinch stimuli had high mechanical thresholds compared to WDR neurons activated also by touch stimuli. The VPM nociceptive neurons were tested with suprathershold graded mechanical stimuli. Most of 21 NS and 8 WDR neurons showed a progressive increase in number of spikes as mechanical stimulus intensity was increased. In some neurons, the responses reached a peak before the highest intensity was given. Application of 5 mM CoCl₂ (10 µl) solution to the trigeminal subnucleus caudalis did not produce any significant changes in the spontaneous activity, RF size, mechanical threshold, and response to suprathresold mechanical stimuli of 9 VPM nociceptive neurons tested.

17 of 33 VPM nociceptive neurons responded to noxious heat as well as noxious mechanical stimuli applied to their RF. Application of the mustard oil, a small-fiber excitant and inflammatory irritant, to the right maxillary first molar tooth pulp induced an immediate but short-lasting neuronal discharges upto approximately 4 min in 16 of 42 VPM nociceptive neurons.

These results suggest that VPM thalamic nucleus may contribute to the sensory discriminative aspect of orofacial nociception.
Keywords: VPM; orofacial nociception; rat

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Fig. 1

Location of the histologically confirmed recording sites plotted on the diagram of ventral posteromedial thalamic (VPM) nucleus. Coronal section of rat brain at 3.3 mm posterior to the Bregma (Paxinos and Watson, 1998). Filled circles show the location of nociceptive specific neurons, whereas open circles show the location of wide dynamic range neurons. VPM, ventral posteromedial thalamic nucleus; VPL, ventral posterolateral thalamic nucleus; PO, posterior thalamic nuclei; ic, internal capsule; mt, mammillothalamic tract; f, fornix.

Fig. 2

Example of receptive field (RF) and response properties of VPM nociceptive neuron. A: nociceptive specific neuron, B: wide dynamic range neuron. RF: The dot represents the spot from which the neuron could be activated. Threshold: Line over the action potentials showing the mechanical force applied to the RF. Pinch response: The stimulus-response curve (force vs firing rate) of neuron. RH: Peristimulus time histogram (PSTH) showing the response to radiant heat applied to the RF. The bar indicates the duration (3 sec) of the stimulus. MO: PSTH showing the response to mustard oil (MO) applied into the right maxillary first molar pulp. The arrow indicates the time of MO application.

Fig. 3

Histogram showing percentage of ventral posteromedial thalamic (VPM), trigeminal subnucleus caudalis (Vc) and oralis (Vo) nociceptive neurons having a mechanoreceptive field limited within one V division (1 DIV) or involving two (2 DIV) or all three trigeminal divisions (3 DIV), and a mechanoreceptive field involving intraoral (IO) region. A: NS neuron, B: WDR neuron. Vc data reported by Hu, J.W., Pain, 1990. Vo data reported by Park et al., J. Neurophysiol. 2001.

Fig. 4

The dot raster display showing response of a VPM WDR neuron to repetitive (1 Hz, 1 mA, 0.2 ms or 2 ms) electrical stimulation of its receptive field. A single dot represents the occurrence of a single action potential; rows represent successive responses shown from top (first stimulus) to bottom (20th stimulus). Note the "wind-up" of the neuron's C fiber evoked responses to successive electrical stimuli in lower trace.

Fig. 5

Distribution of mechanical threshold of individual VPM nociceptive neurons. A: NS neuron (n=32), B: WDR neuron (n=12). Inset shows mean mechanical threshold ± S.E.

Fig. 6

Stimulus-response curve of individual VPM nociceptive neuron to graded mechanical stimuli. A: NS neuron (n=21), B: WDR neuron (n=8). Mean stimulus-response curve is drawn with the thick line. Note that WDR and NS neurons showed a progressive increase in number of spikes as mechanical stimulus intensity was increased.

Table 2

Changes in RF and neuronal response properties of VPM nociceptive neurons following application of CoCl₂ or saline to trigeminal subnucleus caudalis in adult rats

All values are shown as mean ± S.E. Note that RF and neuronal response properties are not significantly changed after CoCl₂ or saline application (Wilcoxon signed rank test).

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Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat

J Korean Acad Conserv Dent. 2002;27(6):587-599. Published online November 30, 2002

DOI: https://doi.org/10.5395/JKACD.2002.27.6.587

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Figure

Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat

Fig. 1 Location of the histologically confirmed recording sites plotted on the diagram of ventral posteromedial thalamic (VPM) nucleus. Coronal section of rat brain at 3.3 mm posterior to the Bregma (Paxinos and Watson, 1998). Filled circles show the location of nociceptive specific neurons, whereas open circles show the location of wide dynamic range neurons. VPM, ventral posteromedial thalamic nucleus; VPL, ventral posterolateral thalamic nucleus; PO, posterior thalamic nuclei; ic, internal capsule; mt, mammillothalamic tract; f, fornix.

Fig. 2 Example of receptive field (RF) and response properties of VPM nociceptive neuron. A: nociceptive specific neuron, B: wide dynamic range neuron. RF: The dot represents the spot from which the neuron could be activated. Threshold: Line over the action potentials showing the mechanical force applied to the RF. Pinch response: The stimulus-response curve (force vs firing rate) of neuron. RH: Peristimulus time histogram (PSTH) showing the response to radiant heat applied to the RF. The bar indicates the duration (3 sec) of the stimulus. MO: PSTH showing the response to mustard oil (MO) applied into the right maxillary first molar pulp. The arrow indicates the time of MO application.

Fig. 3 Histogram showing percentage of ventral posteromedial thalamic (VPM), trigeminal subnucleus caudalis (Vc) and oralis (Vo) nociceptive neurons having a mechanoreceptive field limited within one V division (1 DIV) or involving two (2 DIV) or all three trigeminal divisions (3 DIV), and a mechanoreceptive field involving intraoral (IO) region. A: NS neuron, B: WDR neuron. Vc data reported by Hu, J.W., Pain, 1990. Vo data reported by Park et al., J. Neurophysiol. 2001.

Fig. 4 The dot raster display showing response of a VPM WDR neuron to repetitive (1 Hz, 1 mA, 0.2 ms or 2 ms) electrical stimulation of its receptive field. A single dot represents the occurrence of a single action potential; rows represent successive responses shown from top (first stimulus) to bottom (20th stimulus). Note the "wind-up" of the neuron's C fiber evoked responses to successive electrical stimuli in lower trace.

Fig. 5 Distribution of mechanical threshold of individual VPM nociceptive neurons. A: NS neuron (n=32), B: WDR neuron (n=12). Inset shows mean mechanical threshold ± S.E.

Fig. 6 Stimulus-response curve of individual VPM nociceptive neuron to graded mechanical stimuli. A: NS neuron (n=21), B: WDR neuron (n=8). Mean stimulus-response curve is drawn with the thick line. Note that WDR and NS neurons showed a progressive increase in number of spikes as mechanical stimulus intensity was increased.

Fig. 1

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Fig. 6

Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat

Table 2

Changes in RF and neuronal response properties of VPM nociceptive neurons following application of CoCl₂ or saline to trigeminal subnucleus caudalis in adult rats

All values are shown as mean ± S.E. Note that RF and neuronal response properties are not significantly changed after CoCl₂ or saline application (Wilcoxon signed rank test).

Table 2 Changes in RF and neuronal response properties of VPM nociceptive neurons following application of CoCl2 or saline to trigeminal subnucleus caudalis in adult rats

All values are shown as mean ± S.E. Note that RF and neuronal response properties are not significantly changed after CoCl₂ or saline application (Wilcoxon signed rank test).