Imbalance Between Excitatory and Inhibitory Synaptic Transmission in the Primary Somatosensory Cortex Caused by Persistent Nociception in Rats

Abstract

There is substantial evidence supporting the notion that the primary somatosensory (S1) cortex is an important structure involved in the perceptional component of pain. However, investigations have mainly focused on other pain-related formations, and few reports have been provided to investigate the synaptic plasticity in the S1 cortex in response to persistent pain. In the present study, we report that bee venom (BV) injection triggered an imbalance between excitatory and inhibitory synaptic transmission in the S1 cortex in rats. Using a multi-electrode array recording, we found that BV-induced persistent inflammatory pain led to temporal and spatial enhancement of synaptic plasticity. Moreover, slice patch clamp recordings on identified pyramidal neurons demonstrated that BV injection increased presynaptic and postsynaptic transmission in excitatory synapses and decreased postsynaptic transmission in inhibitory synapses in the layer II/III neurons within the S1 cortex. In immunohistochemistry and Western blot sections, the distribution and expression of total AMPA receptor subunits and gamma-amino butyric acid-A (GABA_A) were unaffected, although the membrane fractions of GluR2 and GABA_A were decreased, and their cytosolic fractions were increased in contrast. The change of GluR1 was opposite to that of GluR2, and GluR3 did not change significantly. Our studies, therefore, provide direct evidence for both presynaptic and postsynaptic changes in synapses within the S1 cortex in persistent nociception, which are probably related to the membrane trafficking of GluR1, GluR2, and GABA_A. Perspective: Increased synaptic plasticity was detected in S1 after peripheral nociception, with enhanced excitatory and decreased inhibitory synaptic transmissions. Increased GluR1, and decreased GABA_Aα1 and GluR2 membrane trafficking were detected. Therefore, the disrupted excitatory/inhibitory balance in transmissions is involved in nociception processing, and S1 can be a potential antinociceptive site.

Keywords: AMPA receptor; GABA receptor; Primary somatosensory cortex; bee venom test; multi-electrode array; synaptic plasticity.