Glutamate/GABA balance in ACC modulates the nociceptive responses of vocalization: An expression of affective-motivational component of pain in guinea pigs

Physiology and Behavior

Volumn 126, Issue , 2014, Pages 8-14

  Zugaib, João ^a   Coutinho, Márcio Ramos ^a   Ferreira, Mateus Dalbem ^a   Menescal de Oliveira, Leda ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

GABA; Glutamate; Guinea pig; Nociception; Vocalization

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; DIZOCILPINE; GLUTAMIC ACID; HOMOCYSTEIC ACID; MUSCIMOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMPLITUDE MODULATION; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; GABAERGIC SYSTEM; GUINEA PIG; MALE; MICROINJECTION; MOTIVATION; NEUROMODULATION; NEUROTRANSMISSION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PRIORITY JOURNAL; STIMULUS RESPONSE; VOCALIZATION;

GABA; GLUTAMATE; GUINEA PIG; NOCICEPTION; VOCALIZATION;

ANIMALS; BICUCULLINE; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGENTS; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GUINEA PIGS; GYRUS CINGULI; HOMOCYSTEINE; MALE; MICROINJECTIONS; MUSCIMOL; PAIN; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 84892646461     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.12.004     Document Type: Article

References (51)

1. Bryant R.A., Felmingham K., Whitford T.J., Kemp A., Hughes G., Peduto A., et al. Rostral anterior cingulate volume predicts treatment response to cognitive-behavioural therapy for posttraumatic stress disorder. J Psychiatry Neurosci 2008, 33:142-146.
2. Chua P., Krams M., Toni I., Passingham R., Dolan R. A functional anatomy of anticipatory anxiety. Neuroimage 1999, 9:563-571.
3. Frankland P.W., Bontempi B., Talton L.E., Kaczmarek L., Silva A.J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 2004, 304(5672):881-883.
4. Coutinho M.R., Menescal-de-Oliveira L. Role of homocysteic acid in the guinea pig (Cavia porcellus) anterior cingulate cortex in tonic immobility and the influence of NMDA receptors on the dorsal PAG. Behav Brain Res 2010, 208:237-242.
5. Johansen J.P., Fields H.L., Manning B.H. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci U S A 2001, 98:8077-8082.
6. Johansen J.P., Fields H.L. Glutamatergic activation of anterior cingulated cortex produces an aversive teaching signal. Nat Neurosci 2004, 7:398-403.
7. Lei L.G., Sun S., Gao Y.J., Zhao Z.Q., Zhang Y.Q. NMDA receptors in the anterior cingulate cortex mediate pain-related aversion. Exp Neurol 2004, 189:413-421.
8. Wang H., Ren W.H., Zhang Y.Q., Zhao Z.Q. GABAergic disinhibition facilitates polysynaptic excitatory transmission in rat anterior cingulate cortex. Biochem Biophys Res Commun 2005, 338:1634-1639.
9. Zhang Z., Séguéla P. Metabotropic induction of persistent activity in layers II/III of anterior cingulated cortex. Cereb Cortex 2010, 20:2948-2957.
10. Bozkurt A., Zilles K., Schleicher A., Kamper L., Arigita E.S., Uylings H.B. Distributions of transmitter receptors in the macaque cingulate cortex. Neuroimage 2005, 25:219-229.
11. LaGraize S.C., Fuchs P.N. GABAa but not GABAb receptors in the rostral anterior cingulate cortex selectively modulate pain-induced escape/avoidance. Behav Exp Neurol 2007, 204:182-194.
12. Menescal-de-Oliveira L., Lico M.C. Pain modulation in the adrenergically stimulated area postrema in the alert guinea pig. Physiol Behav 1977, 19:359-364.
13. Menescal-de-Oliveira L., Hoffmann A. The parabrachial region as a possible region modulating simultaneously pain and tonic immobility. Behav Brain Res 1993, 56:127-132.
14. Favaroni-Mendes L.A., Menescal-de-Oliveira L. Role of cholinergic, opioidergic and GABAergic neurotransmission of the dorsal hippocampus in the modulation of nociception in guinea pigs. Life Sci 2008, 83:644-650.
15. da Silva L.F.S., Coutinho M.R., Menescal-de-Oliveira L. Opioidergic and GABAergic mechanisms in the rostral ventromedial medulla modulate the nociceptive response of vocalization in guinea pigs. Brain Res Bull 2010, 82:177-183.
16. da Silva L.F.S., Coimbra N.C., Menescal-de-Oliveira L. rostral ventromedial medulla modulates nociception and tonic immobility behavior through connections with the A7 catecholaminergic region. Behav Brain Res 2012, 233:422-427.
17. Jürgens U., Pratt R. Role of the periaqueductal grey in vocal expression of emotion. Brain Res 1979, 167:367-378.
18. Borszcz G.S. Increases in vocalization and motor reflex thresholds are influenced by the site of morphine microinjection: comparisons following administration into the periaqueductal gray, ventral medulla, and spinal subarachnoid space. Behav Neurosci 1995, 109:502-522.
19. Sanchéz C. Stress-induced vocalization in adult animals. A valid model of anxiety?. Eur J Pharmacol 2003, 463:133-143.
20. Bandler R., Shipley M.T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?. Trends Neurosci 1994, 17:379-389.
21. Borszcz G.S. Pavlovian conditional vocalizations of the rat: a model system for analyzing the fear of pain. Behav Neurosci 1995, 109:648-662.
22. Carrive P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav Brain Res 1993, 58:27-47.
23. Jürgens U. The neural control of vocalization in mammals: a review. J Voice 2009, 23:1-10.
24. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
25. Rössner W. Stereotaktischer hirnatlas vom meerschweinchen 1965, Pallas Verlag, Munich.
26. Cao H., Gao Y.J., Ren W.H., Li T.T., Duan K.Z., Cui Y.H., et al. Activation of extracellular signal-regulated kinase in the anterior cingulate cortex contributes to the induction and expression of affective pain. J Neurosci 2009, 29:3307-3321.
27. Donahue R.R., LaGraize S.C., Fuchs P.N. Electrolytic lesion of the anterior cingulate cortex decreases inflammatory, but not neuropathic nociceptive behavior in rats. Brain Res 2001, 897:131-138.
28. Lee D.E., Kim S.J., Zhuo M. Comparison of behavioral responses to noxious cold and heat in mice. Brain Res 1999, 845:117-121.
29. Kang S.J., Liu M.G., Chen T., Ko H.G., Baek G.C., Lee H.R., et al. Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. J Neurosci 2012, 32:11318-11329.
30. Wu L.J., Zhao M.G., Toyoda H., Ko S.W., Zhuo M. Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurosci 2005, 94:1805-1813.
31. Li T.T., Ren W.H., Xio X., Nan J., Cheng L.Z., Zhang X.H., et al. NMDA NR2A and NR2B receptors in the rostral anterior cingulate cortex contribute to pain-related aversion in male rats. Pain 2009, 146:183-193.
32. Wei F., Li P., Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999, 19:9346-9354.
33. Calejesan A.A., Kim S.J., Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 2000, 4:83-96.
34. López-Avila A., Coffeen U., Ortega-Legaspi J.M., Del Angel R., Pellicer F. Dopamine and NMDA systems modulae long-term nociception in rat anterior cingulate córtex. Pain 2004, 111:136-143.
35. Harte S.E., Spuz C.A., Borszcz G.S. Functional interaction between medial thalamus and rostral anterior cingulate cortex in the suppression of pain affect. Neuroscience 2011, 172:460-473.
36. Andrews P.R., Johnston G.A.R. Gaba agonists and antagonists. Biochem Pharmacol 1979, 28:2697-2702.
37. 3H] gaba binding to rat brain synaptic membranes by bicuculline related alkaloids. Biochem Pharmacol 1984, 33:3537-3545.
38. Chebib M., Johnston G.A.R. The 'ABC' of GABA receptors: a brief review. Clin Exp Pharmacol Physiol 1999, 26:937-940.
39. Xu H., Wu L.J., Wang H., Zhang X., Vadakkan K.I., Kim S.S., et al. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 2008, 28:7445-7453.
40. Gong K.R., Cao F.L., He Y., Gao C.Y., Wang D.D., Li H., et al. Enhanced excitatory and reduced inhibitory synaptic transmission contribute to persistent pain-induced neuronal hyper-responsiveness in anterior cingulate cortex. Neuroscience 2010, 171:1314-1325.
41. Higashi H., Tanaka E., Nishi S. Synaptic responses of guinea pig cingulate cortical neurons in vitro. J Neurophysiol 1991, 65:822-833.
42. Zhuo M. Central inhibition and placebo analgesia. Mol Pain 2005, 21:1-4.
43. Zhang L., Zhang Y., Zhao Z.Q. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur J Neurosci 2005, 22:1141-1148.
44. Cohen S., Greenberg M.E. Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 2008, 24:183-209.
45. Rebola N., Srikumar B.N., Mulle C. Activity-dependent synaptic plasticity of NMDA receptors. J Physiol 2010, 588:93-99.
46. Hara M.R., Snyder S.H. Cell signaling and neuronal death. Annu Rev Pharmacol Toxicol 2007, 47:117-141.
47. Petralia R.S. Distribution of extrasynaptic NMDA receptors on neurons. Sci World J 2012, 2012:1-11.
48. Qu C., King T., Okun A., Lai J., Fields H.L., Porreca F. Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy. Pain 2011, 152:1641-1648.
49. Ortega-Legaspi J.M., Avila A.L., Coffeen U., Angel R., Pellicer F. Scopolamine into the anterior cingulate cortex diminishes nociception in a neuropathic pain model in the rat: an interruption of "nociception-related memory acquisition"?. Eur J Pain 2003, 7:425-429.
50. Zubieta J.K., Ketter T.A., Bueller J.A., Xu Y., Kilbourn M.R., Young E.A., et al. Regulation of human affective responses by anterior cingulate and limbic mu-opioid neurotransmission. Arch Gen Psychiatry 2003, 60:1145-1153.
51. Leite-Panissi C.R., Rodrigues C.L., Brentegani M.R., Menescal-de-Oliveira L. Endogenous opiate analgesia induced by tonic immobility in guinea pigs. Braz J Med Biol Res 2000, 34:245-250.