Was it a pain or a sound? Across-species variability in sensory sensitivity.
Natural selection has shaped the physiological properties of sensory systems across species, yielding large variations in their sensitivity. Here, we used laser stimulation of skin nociceptors, a widely used technique to investigate pain in rats and humans, to provide a vivid example of how ignoring these variations can lead to serious misconceptions in sensory neuroscience. In 6 experiments, we characterized and compared the physiological properties of the electrocortical responses elicited by laser stimulation in rats and humans. We recorded the electroencephalogram from the surface of the brain in freely moving rats and from the scalp in healthy humans. Laser stimuli elicited 2 temporally distinct responses, traditionally interpreted as reflecting the concomitant activation of different populations of nociceptors with different conduction velocities: small-myelinated Aδ-fibres and unmyelinated C-fibres. Our results show that this interpretation is valid in humans, but not in rats. Indeed, the early response recorded in rats does not reflect the activation of the somatosensory system, but of the auditory system by laser-generated ultrasounds. These results have wide implications: retrospectively, as they prompt for a reconsideration of a large number of previous interpretations of electrocortical rat recordings in basic, preclinical, and pharmacological research, and prospectively, as they will allow recording truly pain-related cortical responses in rats.
Key Laboratory of Cognition and Personality (Ministry of Education) and Faculty of Psychology, Southwest University, Chongqing, China Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
Li
L
Hu
Xiaolei L
XL
Xia
Weiwei W
WW
Peng
Wenxin X
WX
Su
Fei
F
Luo
Hong
H
Yuan
Antao T
AT
Chen
Meng
M
Liang
Giandomenico
G
Iannetti
D000818:Animals; D001307:Auditory Perception / Q000502:physiology*; D002540:Cerebral Cortex / Q000502:physiology*; D004569:Electroencephalography; D005072:Evoked Potentials, Auditory / Q000502:physiology*; D005073:Evoked Potentials, Somatosensory / Q000502:physiology*; D005260:Female; D006801:Humans; D007834:Lasers; D008297:Male; D009413:Nerve Fibers, Myelinated / Q000502:physiology; D036421:Nerve Fibers, Unmyelinated / Q000502:physiology; D009619:Nociceptors / Q000502:physiology*; D058748:Pain Perception / Q000502:physiology*; D010812:Physical Stimulation; D051381:Rats; D017207:Rats, Sprague-Dawley; D012867:Skin / Q000294:innervation; D055815:Young Adult