Heterogeneous synaptic inputs from the ventrolateral periaqueductal gray matter to neurons responding to somatosensory stimuli in the rostral ventromedial medulla of rats

The ventrolateral cell column of the midbrain periaqueductal gray matter (vl-PAG) plays a major role in the attenuation of pain behaviour. It is established that this effect is exerted via modulation of neuronal activities in the rostral ventromedial medulla (RVM). Until recently it has been generally accepted that the vl-PAG exerts its modulatory effects upon RVM neurons through a direct monosynaptic pathway. However, recent data suggest that an additional indirect, di- or polysynaptic pathway may also exist. Using in vivo intracellular recordings we tested this hypothesis, by studying synaptic responses of somatosensory receptive RVM neurons evoked by electric stimulation of the vl-PAG in rats. RVM neurons were regarded as somatosensory receptive if they responded to electrical stimulation of the sciatic nerve. Most of the recorded RVM cells were excited by vl-PAG stimulation. Some of them responded with a short onset latency (3.6+/-0.9 ms) corresponding to monosynaptic excitation. All of these neurons were also excited by sciatic nerve stimulation at nociceptive intensities. In contrast to this, another proportion of the recorded RVM neurons responded with a four times longer (14.8+/-3 ms) onset latency to the vl-PAG stimulation, corresponding to polysynaptic modulation. All of these neurons were inhibited by sciatic nerve stimulation. The findings show that RVM neurons receive heterogeneous monosynaptic and polysynaptic inputs from the vl-PAG. The results also suggest that the monosynaptic and polysynaptic pathways modulate the activity of functionally distinct groups of RVM neurons.