Journal of Neuroscience, Vol 7, 547-564, Copyright © 1987 by Society for Neuroscience
Response properties of nociceptive and low-threshold mechanoreceptive neurons in the hamster superior colliculus
MA Larson, JG McHaffie and BE Stein
There are many somatosensory neurons in the hamster superior colliculus
(SC); some respond to innocuous tactile stimuli, while others respond
either preferentially, or solely, to noxious stimuli. Yet, there are little
quantitative data describing the responses of these neurons. We sought to
provide such information by relating stimulus intensity to the magnitude of
the neural response using controlled innocuous and noxious mechanical and
thermal stimuli. Of 122 somatosensory SC neurons studied in
urethane-anesthetized hamsters, the majority (52%) had low- threshold
mechanoreceptive properties (LT). LT neurons had force thresholds less than
1 gm, adapted rapidly to maintained stimuli, and did not respond with
higher numbers of impulses to noxious mechanical or thermal stimuli. A
smaller, though substantial, proportion of neurons (45%) responded either
preferentially, or solely, to noxious stimuli. A few neurons (3%) were
inhibited by either light tactile or noxious mechanical stimuli. Two
populations of nociceptive neurons were found and classified either as wide
dynamic range (WDR) neurons (n = 25), those that responded to gentle
mechanical, noxious mechanical, and/or thermal stimuli; or
nociceptive-specific (NS) neurons (n = 30), those that responded solely to
high-intensity mechanical or noxious thermal stimuli. WDR neurons responded
monotonically to increases in the intensity of innocuous mechanical
stimuli, and displacement- response relationship for this population was a
slightly negatively accelerating power function with an exponent of 0.785.
However, the thermal stimulus-response relationships (to graded skin
temperatures) of both WDR and NS neurons were positively accelerating power
functions with exponents of 2.3 and 2.5 (r2 = 0.988), respectively. These
values are consistent with both electrophysiological data from dorsal horn
nociceptive neurons and from human psychophysical results using the same
range of thermal stimuli. These experiments demonstrate that SC neurons are
capable of signaling not only the presence and location of a noxious
stimulus but its intensity as well. Presumably, these neurons play a
significant role in the animal's reactions to potentially harmful stimuli.
The partial laminar segregation of WDR and NS neurons may reflect different
involvements of particular nociceptive subtypes in the various overt
responses mediated by the SC.