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Quantitative characterization of low-threshold mechanoreceptor inputs to lamina I spinoparabrachial neurons in the rat.

Andrew D - J. Physiol. (Lond.) (2009)

Bottom Line: Graded velocity brushing stimuli (6.6-126 cm s(-1)) were used to characterize the mechanoreceptor inputs to 'wide dynamic range' neurons in lamina I of the dorsal horn that had axons that projected to the contralateral parabrachial nucleus.The most effective tactile stimuli for activation of 'wide dynamic range' lamina I spinoparabrachial neurons were low velocity brush strokes: peak discharge occurred at a mean velocity of 9.2 cm s(-1) (range 6.6-20.4 cm s(-1), s.d. 5.0 cm s(-1)), and declined exponentially as brush velocity increased.The data indicate that C-fibres, but not A-fibres, conveyed low-threshold mechanoreceptor inputs to lamina I projection neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Oral & Maxillofacial Surgery, School of Clinical Dentistry, Claremont Crescent, Sheffield S10 2TA, UK. d.andrew@sheffield.ac.uk

ABSTRACT
It has been suggested that primary afferent C-fibres that respond to innocuous tactile stimuli are important in the sensation of pleasurable touch. Although it is known that C-tactile fibres terminate in the substantia gelatinosa (lamina II) of the spinal cord, virtually all of the neurons in this region are interneurons, and currently it is not known how impulses in C-mechanoreceptors are transmitted to higher centres. In the current study, I have tested the quantitative response properties of 'wide dynamic range' projection neurons in lamina I of the spinal cord to graded velocity brushing stimuli to identify whether low-threshold mechanoreceptor input to these neurons arises from myelinated or umyelinated nerve fibres. Graded velocity brushing stimuli (6.6-126 cm s(-1)) were used to characterize the mechanoreceptor inputs to 'wide dynamic range' neurons in lamina I of the dorsal horn that had axons that projected to the contralateral parabrachial nucleus. The most effective tactile stimuli for activation of 'wide dynamic range' lamina I spinoparabrachial neurons were low velocity brush strokes: peak discharge occurred at a mean velocity of 9.2 cm s(-1) (range 6.6-20.4 cm s(-1), s.d. 5.0 cm s(-1)), and declined exponentially as brush velocity increased. The data indicate that C-fibres, but not A-fibres, conveyed low-threshold mechanoreceptor inputs to lamina I projection neurons.

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Identification of ‘wide dynamic range’ lamina I spinoparabrachial neurons in vivoA, pair of traces showing 1-for-1 following of a train of 6 antidromic electrical stimuli (40 μA, 1 ms, 250 Hz; vertical ticks) delivered from a stimulating electrode in the contralateral parabrachial nucleus. The conduction distance was 87 mm. B, collision of the first antidromic impulse in a train of 3 (150 Hz, upper trace) when an orthodromic impulse (asterisk, lower trace) occurred within the critical interval. The arrowhead indicates the point at which the first antidromic response should have occurred. Vertical ticks indicate the timing of the antidromic stimuli. C, peri-stimulus time histogram showing the response of the neuron shown above to innocuous (brushing with a hand-held brush; velocity ∼1 cm s−1) and noxious mechanical stimuli. D, histogram showing the response of the same neuron to graded cooling stimuli, applied with a feedback-controlled Peltier element. E, response of the same unit to graded heat.
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fig01: Identification of ‘wide dynamic range’ lamina I spinoparabrachial neurons in vivoA, pair of traces showing 1-for-1 following of a train of 6 antidromic electrical stimuli (40 μA, 1 ms, 250 Hz; vertical ticks) delivered from a stimulating electrode in the contralateral parabrachial nucleus. The conduction distance was 87 mm. B, collision of the first antidromic impulse in a train of 3 (150 Hz, upper trace) when an orthodromic impulse (asterisk, lower trace) occurred within the critical interval. The arrowhead indicates the point at which the first antidromic response should have occurred. Vertical ticks indicate the timing of the antidromic stimuli. C, peri-stimulus time histogram showing the response of the neuron shown above to innocuous (brushing with a hand-held brush; velocity ∼1 cm s−1) and noxious mechanical stimuli. D, histogram showing the response of the same neuron to graded cooling stimuli, applied with a feedback-controlled Peltier element. E, response of the same unit to graded heat.

Mentions: Recordings were made from 95 antidromically-identified lamina I spinoparabrachial neurons, of which 10 were activated by low-threshold mechanical stimulation. All of these 10 neurons were, in addition to being activated by brushing, also activated by noxious mechanical (pinching with smooth-tipped forceps) and noxious heat stimuli, but none was excited by graded intensity cooling/cold (4–31°C) stimuli. The discharge of all 10 units increased as the stimulus intensity increased from innocuous to noxious, and they were therefore classified as ‘wide dynamic range’ neurons (Mendell, 1966; Fig. 1). No neurons were encountered that were exclusively activated by tactile stimuli, similar to other studies of lamina I spinoparabrachial neurons (Bester et al. 2000; Keller et al. 2007). The central conduction velocities of these ‘wide dynamic range’ lamina I spinoparabrachial neurons were in the range 5.9–25.0 m s−1 (mean 13.0 m s−1, s.d. 5.8 m s−1), which is significantly faster than the conduction velocities of nociceptive-specific lamina I spinoparabrachial neurons (P < 0.02, unpaired t test; Andrew, 2009). ‘Wide dynamic range’ neurons had low levels of ongoing (background) activity, with the average being 0.05 impulses s−1 (range 0–0.14, s.d. 0.1) over a 1 min recording period at room temperature, prior to quantitative characterization. All of the receptive fields of the neurons reported here included both hairy and glabrous skin, but low-threshold responses were only evoked from hairy skin. Receptive field sizes covered a broad range with the smallest covering just a single digit and the largest extending across the whole ventral and lateral surface of the hindpaw. However, the mean receptive field size of ‘wide dynamic range’ lamina I spinoparabrachial neurons (160 mm2, range 42–327 mm2, s.d. 124 mm2) tended to be larger than those of nociceptive-specific lamina I spinoparabrachial neurons (mean 83 mm2, range 16–197 mm2, s.d. 72 mm2). Receptive field organization was comparable to other studies of lamina I projection neurons (e.g. Ferrington et al 1987): a small, high sensitivity zone where both low- and high-threshold stimuli were effective, surrounded by a larger region of lower sensitivity where only noxious stimuli evoked responses. The anatomical sites of terminations of the axons of wide dynamic range lamina I spinoparabrachial neurons were comparable to the population of lamina I spinoparabrachial neurons as a whole (Andrew, 2009): 90% of neurons were activated from the internal lateral subnucleus, 80% from the external lateral subnucleus and 70% from the Kölliker–Fuse nucleus.


Quantitative characterization of low-threshold mechanoreceptor inputs to lamina I spinoparabrachial neurons in the rat.

Andrew D - J. Physiol. (Lond.) (2009)

Identification of ‘wide dynamic range’ lamina I spinoparabrachial neurons in vivoA, pair of traces showing 1-for-1 following of a train of 6 antidromic electrical stimuli (40 μA, 1 ms, 250 Hz; vertical ticks) delivered from a stimulating electrode in the contralateral parabrachial nucleus. The conduction distance was 87 mm. B, collision of the first antidromic impulse in a train of 3 (150 Hz, upper trace) when an orthodromic impulse (asterisk, lower trace) occurred within the critical interval. The arrowhead indicates the point at which the first antidromic response should have occurred. Vertical ticks indicate the timing of the antidromic stimuli. C, peri-stimulus time histogram showing the response of the neuron shown above to innocuous (brushing with a hand-held brush; velocity ∼1 cm s−1) and noxious mechanical stimuli. D, histogram showing the response of the same neuron to graded cooling stimuli, applied with a feedback-controlled Peltier element. E, response of the same unit to graded heat.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2821553&req=5

fig01: Identification of ‘wide dynamic range’ lamina I spinoparabrachial neurons in vivoA, pair of traces showing 1-for-1 following of a train of 6 antidromic electrical stimuli (40 μA, 1 ms, 250 Hz; vertical ticks) delivered from a stimulating electrode in the contralateral parabrachial nucleus. The conduction distance was 87 mm. B, collision of the first antidromic impulse in a train of 3 (150 Hz, upper trace) when an orthodromic impulse (asterisk, lower trace) occurred within the critical interval. The arrowhead indicates the point at which the first antidromic response should have occurred. Vertical ticks indicate the timing of the antidromic stimuli. C, peri-stimulus time histogram showing the response of the neuron shown above to innocuous (brushing with a hand-held brush; velocity ∼1 cm s−1) and noxious mechanical stimuli. D, histogram showing the response of the same neuron to graded cooling stimuli, applied with a feedback-controlled Peltier element. E, response of the same unit to graded heat.
Mentions: Recordings were made from 95 antidromically-identified lamina I spinoparabrachial neurons, of which 10 were activated by low-threshold mechanical stimulation. All of these 10 neurons were, in addition to being activated by brushing, also activated by noxious mechanical (pinching with smooth-tipped forceps) and noxious heat stimuli, but none was excited by graded intensity cooling/cold (4–31°C) stimuli. The discharge of all 10 units increased as the stimulus intensity increased from innocuous to noxious, and they were therefore classified as ‘wide dynamic range’ neurons (Mendell, 1966; Fig. 1). No neurons were encountered that were exclusively activated by tactile stimuli, similar to other studies of lamina I spinoparabrachial neurons (Bester et al. 2000; Keller et al. 2007). The central conduction velocities of these ‘wide dynamic range’ lamina I spinoparabrachial neurons were in the range 5.9–25.0 m s−1 (mean 13.0 m s−1, s.d. 5.8 m s−1), which is significantly faster than the conduction velocities of nociceptive-specific lamina I spinoparabrachial neurons (P < 0.02, unpaired t test; Andrew, 2009). ‘Wide dynamic range’ neurons had low levels of ongoing (background) activity, with the average being 0.05 impulses s−1 (range 0–0.14, s.d. 0.1) over a 1 min recording period at room temperature, prior to quantitative characterization. All of the receptive fields of the neurons reported here included both hairy and glabrous skin, but low-threshold responses were only evoked from hairy skin. Receptive field sizes covered a broad range with the smallest covering just a single digit and the largest extending across the whole ventral and lateral surface of the hindpaw. However, the mean receptive field size of ‘wide dynamic range’ lamina I spinoparabrachial neurons (160 mm2, range 42–327 mm2, s.d. 124 mm2) tended to be larger than those of nociceptive-specific lamina I spinoparabrachial neurons (mean 83 mm2, range 16–197 mm2, s.d. 72 mm2). Receptive field organization was comparable to other studies of lamina I projection neurons (e.g. Ferrington et al 1987): a small, high sensitivity zone where both low- and high-threshold stimuli were effective, surrounded by a larger region of lower sensitivity where only noxious stimuli evoked responses. The anatomical sites of terminations of the axons of wide dynamic range lamina I spinoparabrachial neurons were comparable to the population of lamina I spinoparabrachial neurons as a whole (Andrew, 2009): 90% of neurons were activated from the internal lateral subnucleus, 80% from the external lateral subnucleus and 70% from the Kölliker–Fuse nucleus.

Bottom Line: Graded velocity brushing stimuli (6.6-126 cm s(-1)) were used to characterize the mechanoreceptor inputs to 'wide dynamic range' neurons in lamina I of the dorsal horn that had axons that projected to the contralateral parabrachial nucleus.The most effective tactile stimuli for activation of 'wide dynamic range' lamina I spinoparabrachial neurons were low velocity brush strokes: peak discharge occurred at a mean velocity of 9.2 cm s(-1) (range 6.6-20.4 cm s(-1), s.d. 5.0 cm s(-1)), and declined exponentially as brush velocity increased.The data indicate that C-fibres, but not A-fibres, conveyed low-threshold mechanoreceptor inputs to lamina I projection neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Oral & Maxillofacial Surgery, School of Clinical Dentistry, Claremont Crescent, Sheffield S10 2TA, UK. d.andrew@sheffield.ac.uk

ABSTRACT
It has been suggested that primary afferent C-fibres that respond to innocuous tactile stimuli are important in the sensation of pleasurable touch. Although it is known that C-tactile fibres terminate in the substantia gelatinosa (lamina II) of the spinal cord, virtually all of the neurons in this region are interneurons, and currently it is not known how impulses in C-mechanoreceptors are transmitted to higher centres. In the current study, I have tested the quantitative response properties of 'wide dynamic range' projection neurons in lamina I of the spinal cord to graded velocity brushing stimuli to identify whether low-threshold mechanoreceptor input to these neurons arises from myelinated or umyelinated nerve fibres. Graded velocity brushing stimuli (6.6-126 cm s(-1)) were used to characterize the mechanoreceptor inputs to 'wide dynamic range' neurons in lamina I of the dorsal horn that had axons that projected to the contralateral parabrachial nucleus. The most effective tactile stimuli for activation of 'wide dynamic range' lamina I spinoparabrachial neurons were low velocity brush strokes: peak discharge occurred at a mean velocity of 9.2 cm s(-1) (range 6.6-20.4 cm s(-1), s.d. 5.0 cm s(-1)), and declined exponentially as brush velocity increased. The data indicate that C-fibres, but not A-fibres, conveyed low-threshold mechanoreceptor inputs to lamina I projection neurons.

Show MeSH
Related in: MedlinePlus