Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.

<h4>Background</h4>The quantitative end-point for many behavioral tests of nociception is the reaction time, i.e. the time lapse between the beginning of the application of a stimulus, e.g. heat, and the evoked response. Since it is technically impossible to heat the skin instantaneously...

Full description

Bibliographic Details
Main Authors: Jean-Michel Benoist, Ivanne Pincedé, Kay Ballantyne, Léon Plaghki, Daniel Le Bars
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2008-09-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18769624/pdf/?tool=EBI
_version_ 1831676612706304000
author Jean-Michel Benoist
Ivanne Pincedé
Kay Ballantyne
Léon Plaghki
Daniel Le Bars
author_facet Jean-Michel Benoist
Ivanne Pincedé
Kay Ballantyne
Léon Plaghki
Daniel Le Bars
author_sort Jean-Michel Benoist
collection DOAJ
description <h4>Background</h4>The quantitative end-point for many behavioral tests of nociception is the reaction time, i.e. the time lapse between the beginning of the application of a stimulus, e.g. heat, and the evoked response. Since it is technically impossible to heat the skin instantaneously by conventional means, the question of the significance of the reaction time to radiant heat remains open. We developed a theoretical framework, a related experimental paradigm and a model to analyze in psychophysical terms the "tail-flick" responses of rats to random variations of noxious radiant heat.<h4>Methodology/principal findings</h4>A CO(2) laser was used to avoid the drawbacks associated with standard methods of thermal stimulation. Heating of the skin was recorded with an infrared camera and was stopped by the reaction of the animal. For the first time, we define and determine two key descriptors of the behavioral response, namely the behavioral threshold (Tbeta) and the behavioral latency (Lbeta). By employing more than one site of stimulation, the paradigm allows determination of the conduction velocity of the peripheral fibers that trigger the response (V) and an estimation of the latency (Ld) of the central decision-making process. Ld (approximately 130 ms) is unaffected by ambient or skin temperature changes that affect the behavioral threshold (approximately 42.2-44.9 degrees C in the 20-30 degrees C range), behavioral latency (<500 ms), and the conduction velocity of the peripheral fibers that trigger the response (approximately 0.35-0.76 m/s in the 20-30 degrees C range). We propose a simple model that is verified experimentally and that computes the variations in the so-called "tail-flick latency" (TFL) caused by changes in either the power of the radiant heat source, the initial temperature of the skin, or the site of stimulation along the tail.<h4>Conclusions/significance</h4>This approach enables the behavioral determinations of latent psychophysical (Tbeta, Lbeta, Ld) and neurophysiological (V) variables that have been previously inaccessible with conventional methods. Such an approach satisfies the repeated requests for improving nociceptive tests and offers a potentially heuristic progress for studying nociceptive behavior on more firm physiological and psychophysical grounds. The validity of using a reaction time of a behavioral response to an increasing heat stimulus as a "pain index" is challenged. This is illustrated by the predicted temperature-dependent variations of the behavioral TFL elicited by spontaneous variations of the temperature of the tail for thermoregulation.
first_indexed 2024-12-20T04:26:26Z
format Article
id doaj.art-e24f8851918d4c1e8b9392142efe7cf1
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-20T04:26:26Z
publishDate 2008-09-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-e24f8851918d4c1e8b9392142efe7cf12022-12-21T19:53:30ZengPublic Library of Science (PLoS)PLoS ONE1932-62032008-09-0139e312510.1371/journal.pone.0003125Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.Jean-Michel BenoistIvanne PincedéKay BallantyneLéon PlaghkiDaniel Le Bars<h4>Background</h4>The quantitative end-point for many behavioral tests of nociception is the reaction time, i.e. the time lapse between the beginning of the application of a stimulus, e.g. heat, and the evoked response. Since it is technically impossible to heat the skin instantaneously by conventional means, the question of the significance of the reaction time to radiant heat remains open. We developed a theoretical framework, a related experimental paradigm and a model to analyze in psychophysical terms the "tail-flick" responses of rats to random variations of noxious radiant heat.<h4>Methodology/principal findings</h4>A CO(2) laser was used to avoid the drawbacks associated with standard methods of thermal stimulation. Heating of the skin was recorded with an infrared camera and was stopped by the reaction of the animal. For the first time, we define and determine two key descriptors of the behavioral response, namely the behavioral threshold (Tbeta) and the behavioral latency (Lbeta). By employing more than one site of stimulation, the paradigm allows determination of the conduction velocity of the peripheral fibers that trigger the response (V) and an estimation of the latency (Ld) of the central decision-making process. Ld (approximately 130 ms) is unaffected by ambient or skin temperature changes that affect the behavioral threshold (approximately 42.2-44.9 degrees C in the 20-30 degrees C range), behavioral latency (<500 ms), and the conduction velocity of the peripheral fibers that trigger the response (approximately 0.35-0.76 m/s in the 20-30 degrees C range). We propose a simple model that is verified experimentally and that computes the variations in the so-called "tail-flick latency" (TFL) caused by changes in either the power of the radiant heat source, the initial temperature of the skin, or the site of stimulation along the tail.<h4>Conclusions/significance</h4>This approach enables the behavioral determinations of latent psychophysical (Tbeta, Lbeta, Ld) and neurophysiological (V) variables that have been previously inaccessible with conventional methods. Such an approach satisfies the repeated requests for improving nociceptive tests and offers a potentially heuristic progress for studying nociceptive behavior on more firm physiological and psychophysical grounds. The validity of using a reaction time of a behavioral response to an increasing heat stimulus as a "pain index" is challenged. This is illustrated by the predicted temperature-dependent variations of the behavioral TFL elicited by spontaneous variations of the temperature of the tail for thermoregulation.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18769624/pdf/?tool=EBI
spellingShingle Jean-Michel Benoist
Ivanne Pincedé
Kay Ballantyne
Léon Plaghki
Daniel Le Bars
Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
PLoS ONE
title Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
title_full Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
title_fullStr Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
title_full_unstemmed Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
title_short Peripheral and central determinants of a nociceptive reaction: an approach to psychophysics in the rat.
title_sort peripheral and central determinants of a nociceptive reaction an approach to psychophysics in the rat
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18769624/pdf/?tool=EBI
work_keys_str_mv AT jeanmichelbenoist peripheralandcentraldeterminantsofanociceptivereactionanapproachtopsychophysicsintherat
AT ivannepincede peripheralandcentraldeterminantsofanociceptivereactionanapproachtopsychophysicsintherat
AT kayballantyne peripheralandcentraldeterminantsofanociceptivereactionanapproachtopsychophysicsintherat
AT leonplaghki peripheralandcentraldeterminantsofanociceptivereactionanapproachtopsychophysicsintherat
AT daniellebars peripheralandcentraldeterminantsofanociceptivereactionanapproachtopsychophysicsintherat