Summary
Dopamine (DA) utilisation has been determined in the medial bank of the prefrontal cortex (FCx) and the agranular insular cortex (AgCx) of the rat in response to a unilateral reduction of γ-aminobutyric acid (GABA)-mediated inhibition in the thalamic mediodorsal nucleus (MD). The ratios of 3,4-dihydroxyphenylacetic acid (DOPAC) ∶ DA and 4-hydroxy-3-methoxyphenylacetic acid (homovanillic acid, HVA): DA were used as indices of DA utilisation. A bilateral increase in both ratios was found in FCx and AgCx following unilateral infusion of GABA antagonists (1 mM) into MDc. When this concentration was infused into one MDL no change was detected in DA utilisation of FCx, although a bilateral increase was observed in AgCx. However, a correspondence with the known anatomical connections was attained following infusion of lower concentrations (0.5 mM) into MDL in that a significant bilateral elevation of DA utilisation was shown in FCx. The changes induced in these ratios by the above treatments were, in general, due to increases in the concentration of metabolite and slight decreases in that of DA. However, unilateral lesions to the presumed GABA-containing neurones of the rostrodorsal thalamic reticular nucleus (TRNd), which topographically innervate MDL, produced increases in both metabolite and DA concentrations in FCx of both hemispheres, whilst those in AgCx were unaffected. Despite the slightly different results obtained using these two experimental approaches, it is argued that a reduction of tonic GABA-mediated inhibition in MD may tend to activate the DA system in cortical target regions.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Beckstead RM (1976) Convergent thalamic and mesencephalic projections to the anterior medial cortex in the rat. J Comp Neurol 166: 403–416
Beckstead RM (1979) An autoradiographic examination of corticocortical and subcortical projections of the mediodorsalprojection (prefrontal) cortex in the rat. J Comp Neurol 184: 43–62
Benfey M, Bünger UR, Vidal-Sanz M, Bray GM, Aguayo AJ (1985) Axonal regeneration from GABAergic neurons in the adult rat thalamus. J Neurocytol 14: 279–296
Berger B, Thierry AM, Tassin JP, Moyne MA (1976) Dopaminergic innervation of the rat prefrontal cortex: a fluorescence histochemical study. Brain Res 106: 133–145
de Biasi S, Frassoni C, Spreafico R (1986) GABA immunoreactivity in the thalamic reticular nucleus of the rat. A light and electron microscopical study. Brain Res 399: 143–147
Brutus M, Watson Jr. RE Shaikh MB, Siegel HE, Weiner S, Siegel A (1984) A [14C] 2-deoxyglucose analysis of the functional neural pathways of the limbic forebrain in the rat. IV. A pathway from the prefrontal cortical-medial thalamic system to the hypothalamus. Brain Res 310: 279–293
Chéramy A, Chesselet MF, Romo R, Leviel V, Glowinski J (1983) Effects of unilateral electrical stimulation of various thalamic nuclei on the release of dopamine from dendrites and nerve terminals of neurons of the two nigrostriatal dopaminergic pathways. Neuroscience 8: 767–780
Chéramy A, Romo R, Godeheu G, Glowinski J (1984) Effects of electrical stimulation of various midline thalamic nuclei on the bilateral release of dopamine from dendrites and nerve terminals of neurones in the nigro-striatal dopaminergic pathways. Neurosci Lett 44: 193–198
Christoph G, Leonzio RJ, Wilcox KS (1986) Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci 6: 613–619
Commissiong JW (1985) Monoamine metabolites: their relationship and lack of relationship to monoaminergic neuronal activity. Biochem Pharmacol 34: 1127–1131
Cornwall J, Jones MW, Kilpatrick IC, Phillipson OT (1986) Evidence that the thalamic reticular nucleus regulates cerebral cortical dopamine function via the mediodorsal thalamus in the rat. J Physiol 378: 43P
Cornwall J, Phillipson OT (1987) Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport. I. The mediodorsal nucleus. Neuroscience (in press)
Domesick VB (1972) Thalamic relationships of the medial cortex in the rat. Brain Behav Evol 6: 457–483
Enna SJ, Collins JF, Snyder SH (1977) Stereospecificity and structure — activity requirements of GABA receptor binding in rat brain. Brain Res 124: 185–190
Finch DM, Derian EL, Babb TL (1984) Afferent fibres to rat cingulate cortex. Exp Neurol 83: 468–485
Ford APDW, Marsden CA (1986) Influence of anaesthetics on rat striatal dopamine metabolism in vivo. Brain Res 379: 162–166
Gerfen CR, Staines WA, Arbuthnott GW, Fibiger HC (1982) Crossed connections of the substantia nigra in the rat. J Comp Neurol 207: 283–303
Gottesfeld Z, Brandon C, Jacobowitz DM, Wu J-Y (1980) The GABA system in the mammalian habenula. Brain Res Bull 5, Suppl 2: 1–6
Gottesfeld Z, Jacobowitz DM (1978) Further evidence for GABAergic afferents to the lateral habenula. Brain Res 152: 609–613
Guldin WO, Markowitsch HJ (1981) No detectable remote lesions following massive intrastriatal injections of ibotenic acid. Brain Res 225: 446–451
Herkenham M, Nauta WJH (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19–48
Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200: 341–354
Jacobson S, Trojanowski JR (1975) Corticothalamic neurons and thalamocortical terminal fields: an investigation in rat using HRP and autoradiography. Brain Res 85: 385–401
Jones EG (1975) Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162: 285–308
Jones MW, Kilpatrick IC, Phillipson OT (1985) Selective modulation of cerebral cortical dopamine utilisation by the mediodorsal nucleus of the rat thalamus. J Physiol 364: 62P
Jones MW, Kilpatrick IC, Phillipson OT (1986a) Dopamine utilisation in the caudate-putamen and cortex following stimulation of mediodorsal thalamus in the rat. Proc 30th IUPS: 511. 18P
Jones MW, Kilpatrick IC, Phillipson OT (1986b) The agranular insular cortex: a site of unusually high dopamine utilisation. Neurosci Lett 72: 330–334
Jones MW, Kilpatrick IC, Phillipson OT (1987) Regulation of dopamine function in the prefrontal cortex of the rat by the thalamic mediodorsal nucleus. Brain Res Bull 19: 9–17
Kilpatrick IC, Jones MW, Johnson BJ, Cornwall J, Phillipson OT (1986a) Thalamic control of dopaminergic functions in the caudate-putamen of the rat. II. Studies using ibotenic acid injection of the parafascicular-intralaminar nuclei. Neuroscience 19: 979–990
Kilpatrick IC, Jones MW, Phillipson OT (1986b) A semiautomated analysis method for catecholamines, indoleamines, and some prominent metabolites in microdissected regions of the nervous system: an isocratic HPLC technique employing coulometric detection and minimal sample preparation. J Neurochem 46: 1865–1876
Kilpatrick IC, Jones MW, Pycock CJ, Riches I, Phillipson OT (1986c) Thalamic control of dopaminergic functions in the caudate-putamen of the rat. III. The effects of lesions in the parafascicular-intralaminar nuclei on D2 dopamine receptors and high affinity dopamine uptake. Neuroscience 19: 991–1005
Kilpatrick IC, Phillipson OT (1986) Thalamic control of dopaminergic functions in the caudate-putamen of the rat. I. The influence of electrical stimulation of the parafascicular nucleus on dopamine utilisation. Neuroscience 19: 965–978
Kilpatrick IC, Starr MS, Fletcher A, James TA, MacLeod NK (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. I. Behavioural and biochemical studies. Exp Brain Res 40: 45–54
Kilpatrick IC, Starr MS, Summerhayes M (1985) Brain dopamine activity following intranigral or intrathalamic drug injections in the rat. Brain Res Bull 15: 553–561
Köhler C, Schwarcz R (1983) Comparison of ibotenate and kainate neurotoxicity in rat brain: a histological study. Neuroscience 8: 819–835
König JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brain stem. Williams and Wilkins, Baltimore
Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171: 157–192
Leonard CM (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 12: 321–343
Lindvall O, Björklund A, Divac I (1978) Organization of catecholamine neurons projecting to the frontal cortex in the rat. Brain Res 142: 1–24
Lisoprawski A, Herve D, Blanc G, Glowinski J, Tassin JP (1980) Selective activation of the mesocortico-frontal neurons induced by lesion of the habenula in the rat. Brain Res 183: 229–234
McLennan H (1964) The release of acetylcholine and of 3hydroxytyramine from the caudate nucleus. J Physiol 174: 152–161
Minderhoud JM (1971) An anatomical study of the efferent connections of the thalamic reticular nucleus. Exp Brain Res 12: 435–446
Möhler H, Okada T (1977) GABA receptor binding with 3H(+)bicuculline-methiodide in rat CNS. Nature (Lond) 267: 65–67
Montero VM, Scott GL (1981) Synaptic terminals in the dorsal lateral geniculate from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study. Neuroscience 6: 2561–2577
Mulle C, Madariaga A, Deschênes M (1986) Morphology and electrophysiological properties of reticularis thalami neurones in cat: in vivo study of a thalamic pacemaker. J Neurosci 6: 2134–2145
Mushiake S, Shosaku A, Kayama Y (1984) Inhibition of thalamic ventrobasal complex neurons by glutamate infusion into the thalamic reticular nucleus in rats. J Neurosci Res 12: 93–100
Nieoullon A, Chéramy A, Glowinski J (1977) An adaptation of the push-pull cannula method to study the in vivo release of [3H] dopamine synthesised from [3H] tyrosine in the cat caudate nucleus: effects of various physical and pharmacological treatments. J Neurochem 28: 819–828
Nishikawa T, Fage D, Scatton B (1986) Evidence for, and nature of, the tonic inhibitory influence of habenulointerpeduncular pathways upon cerebral dopaminergic transmission in the rat. Brain Res 373: 324–336
Ohara PT, Lieberman AR (1985) The thalamic reticular nucleus of the adult rat: experimental anatomical studies. J Neurocytol 14: 365–411
Ohara PT, Sefton AJ, Lieberman AR (1980) Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat. Brain Res 197: 503–506
Oertel WH, Graybiel AM, Mugnaini E, Elde RP, Schmechel DE, Kopin U (1983) Coexistence of glutamic acid decarboxylase and somatostatin-like immunoreactivity in neurones of the feline nucleus reticularis thalami. J Neurosci 3: 1322–1332
Ottersen O, Storm-Mathisen J (1984) GABA-containing neurons in the thalamus and pretectum of the rodent. An immunocytochemical study. Anat Embryol 170: 197–207
Peschanski M, Villanueva L, Le Bars D, Bernard J-F (1986) Differential metabolic activity in the brain during deep halothane anaesthesia. A qualitative study using [3H] deoxyglucose. Neurosci Lett 71: 1–6
Phillipson OT (1978) Afferent projections to A10 dopaminergic neurons in the rat as shown by the retrograde transport of horseradish peroxidase. Neurosci Lett 9: 353–359
Rebollo Herrero I (1985) Anatomical interrelationships of electrophysiologically identified sites in the ventrobasal thalamus with the somatosensory cortex and the thalamic reticular nucleus in the rat. Ph.D. Thesis, University of Sheffield.
Romo R, Chéramy A, Desban M, Godeheu G, Glowinski J (1983) GABA in the intralaminar thalamic nuclei modulates dopamine release from the two dopaminergic nigro-striatal pathways in the cat. Brain Res Bull 11: 671–680
Sarter M, Markowitsch HJ (1984) Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic, and brain-stem neurones. J Comp Neurol 224: 445–460
Sarter M, Markowitsch HJ (1985) Convergence of intra- and interhemispheric cortical afferents: lack of collateralization and evidence for a subrhinal cell group projecting heterotopically. J Comp Neurol 236: 283–296
Scheibel ME, Scheibel AB (1966) The organization of the nucleus reticularis thalami: a Golgi study. Brain Res 1: 43–62
Schlag J, Waszak M (1970) Characteristics of unit responses in nucleus reticularis thalami. Brain Res 21: 286–288
Siegel A, Fukushima T, Meibach R, Burke L, Edinger H, Weiner S (1977) The origin of the afferent supply to the mediodorsal thalamic nucleus: enhancement of HRP transport by selective lesions. Brain Res 135: 11–23
Skinner JE, Yingling CD (1976) Regulation of slow potential shifts in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. EEG Clin Neurophys 40: 288–296
Starr MS, Kilpatrick IC (1981) Distribution of γ-aminobutyrate in the rat thalamus: specific decreases in thalamic γ-aminobutyrate following lesion or electrical stimulation of the substantia nigra. Neuroscience 6: 1095–1104
Steriade M, Deschênes M (1984) The thalamus as a neuronal oscillator. Brain Res Rev 8: 1–63
Steriade M, Deschênes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54: 1473–1497
Ticku MK, Ban M, Olsen RW (1978) Binding of [3H] α-dihydropicrotoxinin, a γ-aminobutyric acid sy nap tic antagonist, to rat brain. Molec Pharmacol 14: 391–402
Ungerstedt U (1971) Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiologica Scandinavica, Suppl 367: 1–48
Van Eden CG, Hoomeman EMD, Buijs RM, Matthijssen MAH, Geffard M, Uylings HBM (1987) Immunocytochemical localisation of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level. J Comp Neurol (in press)
Van Eden CG, Uylings HBM (1985) Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol 241: 253–267
Vives F, Mogenson GJ (1985) Electrophysiological evidence that the mediodorsal nucleus of the thalamus is a relay between the ventral pallidum and the medial prefrontal cortex in the rat. Brain Res 344: 329–337
Yingling CD, Skinner JE (1975) Regulation of unit activity in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. EEG Clin Neurophys 39: 635–642
Zahm DS, Zaborszky L, Alheid GF, Heimer L (1987) The ventral striato-pallidothalamic projection: II. The ventral pallidothalamic link. J Comp Neurol 255: 592–605
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jones, M.W., Kilpatrick, I.C. & Phillipson, O.T. Dopamine function in the prefrontal cortex of the rat is sensitive to a reduction of tonic GABA-mediated inhibition in the thalamic mediodorsal nucleus. Exp Brain Res 69, 623–634 (1988). https://doi.org/10.1007/BF00247314
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00247314