Physiological influence of lateral proisocortex on the midbrain periaqueductal gray: evidence for a role of an excitatory amino acid in synaptic activation.

Recent anatomical studies in this laboratory have demonstrated that the proisocortex cortex adjacent and dorsal to the rhinal sulcus is one of the major forebrain afferent inputs to the midbrain periaqueductal gray matter in the rat. The physiological influence(s) of this projection has not been examined. The present studies investigated the responses of periaqueductal gray neurons to chemical and electrical stimulation of proisocortex in chloral hydrate-anesthetized rats. In addition, the role of glutamate as a possible transmitter in excitatory proisocortex-periaqueductal gray synaptic responses was tested. Microinjection of D,L-homocysteate into proisocortex excited 44% (19/43), inhibited 37% (16/43) and had no effect on 19% of periaqueductal gray cells. The onset of D,L-homocystic acid-evoked responses ranged from 2 to 60 s; the duration of responses ranged from 1 to 18 min. Low-frequency, single-pulse electrical stimulation of proisocortex robustly altered neuronal discharge in 25% of periaqueductal gray neurons sampled; 10% (74/724) of neurons were excited and 15% (107/724) were inhibited. Insular cortex-evoked excitatory responses had a mean onset latency of 19.5 +/- 4.2 ms and a mean duration of 38.5 +/- 26.9 ms. Inhibitory responses had a mean onset latency of 26.2 +/- 15.6 ms and mean duration of 108.0 +/- 84.9 ms. Trains of high-frequency electrical stimulation of proisocortex excited 22% (13/59) and inhibited 25% (15/59) of periaqueductal gray cells tested. In separate experiments, stimulation electrodes were placed in periaqueductal gray to antidromically activate proisocortex neurons that project to periaqueductal gray.(ABSTRACT TRUNCATED AT 250 WORDS)