M. Michaelis et al., SYMPATHETIC MODULATION OF ACTIVITY IN RAT DORSAL-ROOT GANGLION NEURONS CHANGES OVER TIME FOLLOWING PERIPHERAL-NERVE INJURY, Journal of neurophysiology, 76(2), 1996, pp. 753-763
1. We recorded from centrally connected axons isolated from the proxim
al stump of the sciatic nerve in intact rats and in rats whose nerves
had been transected 4 days-6 mo previously. Afferent axons selected fo
r study had spontaneous impulse activity that originated ectopically i
n dorsal root ganglia (DRGs) L(4) and L(5) The sympathetic supply of t
hese DRGs was excited by repetitive electrical stimulation of ventral
roots T-13 and L(1). We examined quantitatively changes in afferent on
going firing evoked by sympathetic stimulation. Results are based on o
bservations from 161 neurons in rats with sciatic nerve injury and fro
m 58 neurons in control rats with intact sciatic nerves. Of these 219
neurons, 204 had myelinated fibers (A neurons) and 15 had unmyelinated
fibers (C neurons), on the basis of measurements of conduction veloci
ty. 2. In rats with nerve injury the majority of the spontaneously act
ive neurons tested (95 of 161) responded to sympathetic stimulation wi
th a change in ongoing firing frequency: 41 neurons exhibited a signif
icant increase in discharge frequency that was often followed by suppr
ession (28 of 41), and 54 neurons responded with a decrease in ongoing
activity (simple suppression). In control rats, in contrast, only 1 o
f the 58 spontaneously active sensory neurons tested responded to symp
athetic stimulation. 3. In A neurons, the response pattern changed sys
tematically with time after sciatic nerve injury. At 4-22 days after n
erve lesion, excitation was much more common than suppression. At 60-9
3 days, excitation and suppression occurred about equally. At 110-171
days, suppression was by far the more common response. 4. Of the 14 C
neurons, 2 were excited by sympathetic stimulation (at 4-22 days posto
peratively) and 10 were suppressed (2 at 4-22 days, 8 at > 60 days). T
he only spontaneously active C neuron found in control rats was not af
fected by sympathetic stimulation. 5. The magnitude of responses in th
e three postoperative intervals investigated was similar. This was so
for both the excitatory and the simple suppressive responses. The aver
age latency between onset of stimulation and excitatory responses in a
fferent A fibers (similar to 10 s) was significantly less than the lat
ency to simple suppressive responses (similar to 20 s). 6. The mean sp
ontaneous firing rate of A neurons decreased with time after nerve les
ion. No change was observed in C neuron activity. The mean firing rate
of A neurons was significantly higher than that of C neurons 4-93 day
s after nerve lesion, but not later. In all three postoperative period
s investigated, the mean rate of spontaneous activity was the same in
A neurons that responded to sympathetic stimulation and A neurons that
did not. 7. The results show that nerve injury triggers sympathetic-s
ensory coupling within rat DRGs. Excitatory coupling is preferentially
present in the period shortly after nerve injury, and is subsequently
replaced by suppressive coupling. This suggests that there is a gradu
al change in the underlying coupling mechanism.