Physiological influence of lateral proisocortex on the midbrain periaqueductal gray

Evidence for a role of an excitatory amino acid in synaptic activation

M. M. Behbehani, M. Jiang, Matthew Ennis, M. T. Shipley

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

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. Stimulation of periaqueductal gray antidromically activated 10 55 cells at latencies ranging from 7 to 18 ms, and a mean latency of 1 2.0 ± 0.9ms. Assuming a straight line trajectory for proisocortex fibers that project to periaqueductal gray, these values indicate a axonal impulse conduction velocity along proisocortex-periaqueductal gray fibers of 0.6 to 1.4 m/s, with an overall mean of 1.1 m/s. This relatively slow conduction velocity indicates that periaqueductal gray-IC fibers may be thin, unmyelinated axons. Microinjection of the broad-spectrum excitatory amino acid receptor antagonist kynurenic acid directly onto periaqueductal gray neurons blocked proisocortex-evoked excitation in 52% ( 24 46) of periaqueductal gray cells tested. In addition, kynurenic acid blocked inhibitory responses to proisocortex stimulation three of 11 periaqueductal gray cells tested. It is concluded that: 1. (i) proisocortex neurons have a direct synaptic influence on periaqueductal gray neurons. 2. (ii) high-frequency train stimulation or chemical stimulation of proisocortex is significantly more effective in altering the firing pattern of periaqueductal gray neuron than single pulse stimulation, indicating that modulation of periaqueductal gray cells by proisocortex requires some temporal and/or spatial summation. 3. (iii) excitatory amino acid neurotransmission accounted for at least half of the excitatory responses mediated by this afferent system.

Original languageEnglish (US)
Pages (from-to)787-795
Number of pages9
JournalNeuroscience
Volume53
Issue number3
DOIs
StatePublished - Jan 1 1993
Externally publishedYes

Fingerprint

Periaqueductal Gray
Excitatory Amino Acids
Mesencephalon
Neurons
Chemical Stimulation
Electric Stimulation
Kynurenic Acid
Microinjections
Chloral Hydrate
Excitatory Amino Acid Antagonists

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Physiological influence of lateral proisocortex on the midbrain periaqueductal gray : Evidence for a role of an excitatory amino acid in synaptic activation. / Behbehani, M. M.; Jiang, M.; Ennis, Matthew; Shipley, M. T.

In: Neuroscience, Vol. 53, No. 3, 01.01.1993, p. 787-795.

Research output: Contribution to journalArticle

@article{c79139c143cf47838f0512353366046f,
title = "Physiological influence of lateral proisocortex on the midbrain periaqueductal gray: Evidence for a role of an excitatory amino acid in synaptic activation",
abstract = "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. Stimulation of periaqueductal gray antidromically activated 10 55 cells at latencies ranging from 7 to 18 ms, and a mean latency of 1 2.0 ± 0.9ms. Assuming a straight line trajectory for proisocortex fibers that project to periaqueductal gray, these values indicate a axonal impulse conduction velocity along proisocortex-periaqueductal gray fibers of 0.6 to 1.4 m/s, with an overall mean of 1.1 m/s. This relatively slow conduction velocity indicates that periaqueductal gray-IC fibers may be thin, unmyelinated axons. Microinjection of the broad-spectrum excitatory amino acid receptor antagonist kynurenic acid directly onto periaqueductal gray neurons blocked proisocortex-evoked excitation in 52{\%} ( 24 46) of periaqueductal gray cells tested. In addition, kynurenic acid blocked inhibitory responses to proisocortex stimulation three of 11 periaqueductal gray cells tested. It is concluded that: 1. (i) proisocortex neurons have a direct synaptic influence on periaqueductal gray neurons. 2. (ii) high-frequency train stimulation or chemical stimulation of proisocortex is significantly more effective in altering the firing pattern of periaqueductal gray neuron than single pulse stimulation, indicating that modulation of periaqueductal gray cells by proisocortex requires some temporal and/or spatial summation. 3. (iii) excitatory amino acid neurotransmission accounted for at least half of the excitatory responses mediated by this afferent system.",
author = "Behbehani, {M. M.} and M. Jiang and Matthew Ennis and Shipley, {M. T.}",
year = "1993",
month = "1",
day = "1",
doi = "10.1016/0306-4522(93)90624-O",
language = "English (US)",
volume = "53",
pages = "787--795",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",
number = "3",

}

TY - JOUR

T1 - Physiological influence of lateral proisocortex on the midbrain periaqueductal gray

T2 - Evidence for a role of an excitatory amino acid in synaptic activation

AU - Behbehani, M. M.

AU - Jiang, M.

AU - Ennis, Matthew

AU - Shipley, M. T.

PY - 1993/1/1

Y1 - 1993/1/1

N2 - 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. Stimulation of periaqueductal gray antidromically activated 10 55 cells at latencies ranging from 7 to 18 ms, and a mean latency of 1 2.0 ± 0.9ms. Assuming a straight line trajectory for proisocortex fibers that project to periaqueductal gray, these values indicate a axonal impulse conduction velocity along proisocortex-periaqueductal gray fibers of 0.6 to 1.4 m/s, with an overall mean of 1.1 m/s. This relatively slow conduction velocity indicates that periaqueductal gray-IC fibers may be thin, unmyelinated axons. Microinjection of the broad-spectrum excitatory amino acid receptor antagonist kynurenic acid directly onto periaqueductal gray neurons blocked proisocortex-evoked excitation in 52% ( 24 46) of periaqueductal gray cells tested. In addition, kynurenic acid blocked inhibitory responses to proisocortex stimulation three of 11 periaqueductal gray cells tested. It is concluded that: 1. (i) proisocortex neurons have a direct synaptic influence on periaqueductal gray neurons. 2. (ii) high-frequency train stimulation or chemical stimulation of proisocortex is significantly more effective in altering the firing pattern of periaqueductal gray neuron than single pulse stimulation, indicating that modulation of periaqueductal gray cells by proisocortex requires some temporal and/or spatial summation. 3. (iii) excitatory amino acid neurotransmission accounted for at least half of the excitatory responses mediated by this afferent system.

AB - 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. Stimulation of periaqueductal gray antidromically activated 10 55 cells at latencies ranging from 7 to 18 ms, and a mean latency of 1 2.0 ± 0.9ms. Assuming a straight line trajectory for proisocortex fibers that project to periaqueductal gray, these values indicate a axonal impulse conduction velocity along proisocortex-periaqueductal gray fibers of 0.6 to 1.4 m/s, with an overall mean of 1.1 m/s. This relatively slow conduction velocity indicates that periaqueductal gray-IC fibers may be thin, unmyelinated axons. Microinjection of the broad-spectrum excitatory amino acid receptor antagonist kynurenic acid directly onto periaqueductal gray neurons blocked proisocortex-evoked excitation in 52% ( 24 46) of periaqueductal gray cells tested. In addition, kynurenic acid blocked inhibitory responses to proisocortex stimulation three of 11 periaqueductal gray cells tested. It is concluded that: 1. (i) proisocortex neurons have a direct synaptic influence on periaqueductal gray neurons. 2. (ii) high-frequency train stimulation or chemical stimulation of proisocortex is significantly more effective in altering the firing pattern of periaqueductal gray neuron than single pulse stimulation, indicating that modulation of periaqueductal gray cells by proisocortex requires some temporal and/or spatial summation. 3. (iii) excitatory amino acid neurotransmission accounted for at least half of the excitatory responses mediated by this afferent system.

UR - http://www.scopus.com/inward/record.url?scp=0027512056&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0027512056&partnerID=8YFLogxK

U2 - 10.1016/0306-4522(93)90624-O

DO - 10.1016/0306-4522(93)90624-O

M3 - Article

VL - 53

SP - 787

EP - 795

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

IS - 3

ER -