Summary
The areal and laminar distribution of GABAA receptor immunoreactivity was examined in fetal, early postnatal and adult monkey sensory-motor cortex by using a monoclonal antibody to the purified GABAA receptor complex (Vitorica et al. 1988). GABAA receptor immunoreactivity was distributed throughout the neuropil, often outlining the unstained somata of pyramidal and non-pyramidal cells. In all areas of the adult sensory-motor cortex, layers I–IIIA exhibited the most intense immunostaining. In deeper layers of the four cytoarchitectonic fields of the first somatic sensory area (SI), layers IIIB and V were lightly stained and alternated with somewhat more intensely stained layers IV and VI. In deeper layers of area 4, the deeper half of layer IIIA through layer VA was lightly immunostained, but layers VB and VI were slightly more intensely immunoreactive. A variable number of nonpyramidal cell somata in the cortex and underlying white matter showed immunoreactive staining. GABAA receptor immunoreactivity was present throughout the sensory-motor cortex from the youngest fetal age examined (E121), but the pattern of immunostaining differed from that in the adult. In all areas, the densest immunoreactivity was found in a diffuse band in layers III and IV and in the subplate zone. Within the subplate zone, the presence of receptor immunoreactivity and some intensely stained neuronal somata at all fetal ages suggests the presence of a synaptic neuropil. With increasing age, gradual changes in the distribution of receptor immunoreactivity occurred, resulting in an adult-like pattern of immunostaining by postnatal day 1.5. These results show that the laminar pattern of GABAA receptor distribution closely follows the major concentrations of GABA immunoreactive neurons in adults and it is suggested that laminar changes seen in development are associated with the establishment of afferent connections and inhibitory circuits in the sensory-motor cortex.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alloway KD, Burton H (1986) Bicuculline-induced alterations in neuronal responses to controlled tactile stimuli in the second somatosensory cortex of the cat: a microiontophoretic study. Somatosens Res 3:197–211
Barnard EA, Darlison MG, Seeburg P (1987) Molecular biology of the GABAA receptor: the receptor/channel superfamily. Trends Neurosci 10:502–509
Bloom FE, Ueda T, Battenberg E, Greengard P (1979) Immunocytochemical localization in synapses of protein I an endogenous substrate for protein kinases in mammalian brain. Proc Natl Acad Sci USA 76:5982–5986
Blue ME, Parnavelas JG (1983) The formation and maturation of synapses in the visual cortex of rat. II. Quantitative analysis. J Neurocytol 12:697–712
Bowery NG, Price GW, Hudson AL, Hill DR, Wilkin GP, Turnbull MJ (1984) GABA receptor multiplicity: visualization of different receptor types in the mammalian CNS. Neuropharmacol 23:219–231
Cajal S Ramón y (1900) Estudios sobre la corteza cerebral humana. II. Corteza motriz (conclusión). Rev Trimestr Microgr Madrid 5:1–11
Carlson M (1984) Development of tactile discrimination capacity in Macaca mulatta. I. Normal infants. Dev Brain Res 16:69–82
Casalotti SO, Stephenson FA, Barnard EA (1986) Separate subunits for agonist and benzodiazepine binding in the GABAA receptor oligomer. J Biol Chem 261:15 013–15 016
Chalupa LM, Killackey HP (1987) Double-labeled neurons in primary somatosensory cortex (area 3b) of the fetal rhesus monkey. Soc Neurosci Abstr 13:76
Chalupa LM, Killackey HP (1989) Process elimination underlies ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. Proc Natl Acad Sci USA 86:1076–1079
Chudler EH, Pretel S, Kenshalo Jr. DR (1988) Distribution of GAD-immunoreactive neurons in the first (SI) and second (SII) somatosensory cortex of the monkey. Brain Res 456:57–63
Chun JJM, Shatz CJ (1988) Redistribution of synaptic vesicle antiens is correlated with the disappearance of a transient synaptic zone in the developing cerebral cortex. Neuron 1:297–310
Chun JJM, Shatz CJ (1989a) The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci 9:1648–1667
Chun JJM, Shatz CJ (1989b) Interstitial cells of the adult neocortical white matter are the remnant of the early-generated subplate neuron population. J Comp Neurol 282:555–569
Chun JJM, Nakamura MJ, Shatz CJ (1987) Transient cells of the developing mammalian telencephalon are peptide immunoreactive neurons. Nature 325:617–620
Connors BW, Malenka RC, Silva LR (1988) Two inhibitory postsynaptic potentials and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol (London) 406:443–468
Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147–166
Creutzfeldt OD, Ito M (1968) Functional synaptic organisation of primary visual cortex neurones in the cat. Exp Brain Res 6:324–352
de Blas AL, Vitorica J, Friedrich P (1988) Localization of the GABAA receptor in the rat brain with a monoclonal antibody to the 57 000 Mr peptide of the GABAA receptor/benzodiazepine receptor/Cl- channel complex. J Neurosci 8:602–614
De Camilli P, Greengard P (1986) Synapsin I: a synaptic vesicle-associated neuronal phosphoprotein. Biochem Pharmacol 35:4349–4357
DeFelipe J, Jones EG (1985) Vertical organization of γ-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. J Neurosci 5:3246–3260
DeFelipe J, Hendry SHC, Jones EG (1986) A correlative electron microscopic study of basket cells and large GABAergic neurons in the monkey sensory-motor cortex. Neuroscience 17:991–1009
DeFelipe J, Hendry SHC, Jones EG (1989) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res 503:49–54
DeFelipe J, Hendry SHC, Jones EG, Schmechel D (1985) Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J Comp Neurol 231:364–384
Deng L, Ransom RW, Olsen RW (1986) (3H)muscimol photolabels the GABA receptor binding site on a peptide subunit distinct from that labeled with benzodiazepines. Biochem Biophys Res Commun 138:1308–1314
Durham D, Woolsey TA (1985) Functional organization in cortical barrels of normal and vibrissae-damaged mice: a (3H) 2-deoxyglucose study. J Comp Neurol 235:97–110
Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol 52:1066–1093
Enna SJ, (1988) GABA-A receptors. In: Squires RF (ed) GABA and benzodiazepine receptors, Vol. 1. CRC Press Inc, pp 91–106
Ferster D (1986) Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci 6:1284–1301
Ferster D (1987) Origin of orientation-selective EPSPs in simple cells of cat visual cortex. J Neurosci 7:1780–1791
Ferster D (1988) Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. J Neurosci 8:1172–1180
Fitzpatrick D, Lund JS, Schmechel DE, Towles AC (1987) Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. J Comp Neurol 264:73–91
Goldman PS, Nauta WHJ (1977) Columnar distribution of corticocortical fibers in the frontal association, limbic and motor cortex of the developing rhesus monkey. Brain Res 122:393–414
Hand PJ (1982) Plasticity of the rat cortical barrel system. In: Strick PL, Morrison AR (eds) Changing concepts of the nervous system. Academic, New York, pp 49–68
Häring P, Stähli C, Schoch P, Takács B, Staehelin T, Möhler H (1985) Monoclonal antibodies reveal structural homogeneity of γ-aminobutyric acid/benzodiazepine receptors in different brain areas. Proc Natl Acad Sci USA 82:4837–4841
Hendry SHC, Jones EG (1981) Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensorymotor cortex. J Neurosci 4:390–408
Hendry SHC, Jones EG, Emson PC (1984) Morphology, distribution and synaptic relations of somatostatin and neuropeptide Y immunoreactive neurons in rat and monkey neocortex. J Neurosci 5:2254–2268
Hendry SHC, Houser CR, Jones EG, Vaughn JE (1983) Synaptic organization of immimocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12:639–660
Hendry SHC, Jones EG, Killackey HP, Chalupa LM (1987a) Choline acetyltransferase-immunoreactive neurons in fetal monkey cerebral cortex. Dev Brain Res 37:313–317
Hendry SHC, Schwark HD, Jones EG, Yan J (1987b) Numbers and proportions of GABA immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503–1520
Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472
Hendry SHC, Fuchs J, de Blas AL, Jones EG (1990) Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J Neurosci 10:2438–2450
Hicks TP, Dykes RW (1983) Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition. Brain Res 274:160–164
Houser CR, Hendry SHC, Jones EG, Vaughn JE (1983) Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12:617–638
Houser CR, Vaughn JE, Hendry SHC, Jones EG, Peters A (1984) GABA neurons in the cerebral cortex. In: Jones EG, Peters P (eds) Cerebral cortex, Vol 2. Plenum Press, New York, pp 63–89
Houser CR, Olsen RW, Richards JG, Möhler H (1988) Immunohistochemical localization of benzodiazepine/GABAA receptors in the human hippocampal formation. J Neurosci 8:1370–1383
Huntley GW, Jones EG (1990) Cajal-Retzius neurons in developing monkey neocortex show immunoreactivity for calcium binding proteins. J Neurocytol 19:200–212
Huntley GW, Hendry SHC, Jones EG, Chalupa LM, Killackey HP (1987) GABA, neuropeptide and ChaT expression in neurons of the fetal monkey sensory-motor cortex. Soc Neurosci Abstr 13:76
Huntley GW, Hendry SHC, Killackey HP, Chalupa LM, Jones EG (1988) Temporal sequence of neurotransmitter expression by developing neurons of fetal monkey visual cortex. Dev Brain Res 43:69–96
Innocenti GM (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212:824–827
Jones EG (1975a) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160:167–204
Jones EG (1975b) Lamination and differential distribution of thalamic afferents in the sensory-motor cortex of the squirrel monkey. J Comp Neurol 160:167–204
Jones EG (1986) Connectivity of the primate sensory-motor cortex. In: Jones EG, Peters A (eds) Cerebral cortex, Vol 5. Plenum, New York, pp 113–183
Jones EG, Burton H (1976) Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular parietal and temporal regions of primates. J Comp Neurol 168:197–247
Jones EG, Wise SP (1977) Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. J Comp Neurol 175:391–438
Jones EG, Burton H, Porter R (1975) Commissural and corticocortical “columns” in the somatic sensory cortex of primates. Science 190:572–574
Jones EG, Coulter JD, Hendry SHC (1978) Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291–347
Jones EG, DeFelipe J, Hendry SHC, Maggio JE (1988) A study of tachykinin immunoreactive neurons in monkey cerebral cortex. J Neurosci 8:1206–1225
Juliano SL, Whitsel BL (1985) Metabolic labeling associated with index finger stimulation in monkey SI: between animal variability. Brain Res 342–251
Juliano SL, Hand PJ, Whitsel BL (1981) Patterns of increased metabolic activity in somatosensory cortex of monkeys (Macacafascicularis) subjected to controlled cutaneous stimulation: a 2-deoxyglucose study. J Neurophysiol 46:1260–1284
Juliano SL, Whitsel BL, Tommerdahl M, Cheema SS (1989) Determinants of patchy metabolic labeling in the somatosensory cortex of cats: a possible role for intrinsic inhibitory circuitry. J Neurosci 9:1–12
Kelahan AM, Doetsch GS (1984) Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens Res 2:49–81
Kelly JS, Krnjević K, Morris ME, Yim GKW (1969) Anionic permeability of cortical neurones. Exp Brain Res 7:11–31
Killackey HP, Chalupa LM (1986) Ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. J Comp Neurol 244:331–348
Kostović I, Molliver ME (1974) A new interpretation of the laminar development of cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus. Anat Rec 178:395 (Abstr.)
Kostović I, Molliver ME, Van der Loos H (1973) The laminar distribution of synapses in neocortex of fetal dog. Anat Rec 175:362 (Abstr.)
Kuriyama K, Taguchi J (1987) Glycoprotein as a constituent of purified gamma-aminobutyric acid/benzodiazepine receptor complex: structures and physiological roles of its carbohydrate chain. J Neurochem 48:1897–1903
Lidow MS, Goldman-Rakic PS, Gallager DW, Geschwind DH, Rakic P (1990) Distribution of major neurotransmitter receptors in the motor and somatosensory cortex of the rhesus monkey. Neuroscience 32:609–627
Llinás R, McGuiness TL, Leonard CS, Sugimori M, Greengard P (1985) Intraterminal injection of synapsin I or calcium/ calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc Natl Acad Sci USA 82:3035–3039
Lund RD, Mustari MJ (1977) Development of the geniculocortical pathway in rats. J Comp Neurol 173:289–306
Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res 23:167–183
Matthew WD, Tsavaler L, Reichardt LF (1981) Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal neurosecretory tissue. J Cell Biol 91:257–269
McCabe RT, Wamsley JK (1986) Autoradiographic localization of subcomponents of the macromolecular GABA receptor complex. Life Sci 39:1937–1946
Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1984) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224:591–605
Merzenich MM, Recanzone G, Jenkins WM, Allard T, Nudo RJ (1988) Cortical representational plasticity. In: Changeux JP, Konishi M (eds) The neural and molecular basis of learning. John Wiley and Sons, Chichester, England
Molliver ME, Kostović I, Van der Loos H (1973) The development of synapses in cerebral cortex of the human fetus. Brain Res 50:403–407
Olsen RW, Snowhill EW, Wamsley JD (1984) Autoradiographic localization of low affinity GABA receptors with 3H-bicuculline methochloride. Eur J Pharmacol 99:245–247
Palacios JM, Wamsley JK, Kuhar MJ (1981) High affinity GABA receptors: Autoradiographic localization. Brain Res 222:285–307
Penney JB, Pan HS, Young AB, Frey KA, Dauth GW (1981) Quantitative autoradiography of (3H)-muscimol binding in rat brain. Science 214:1036–1038
Prusky GT, Arbuckle JM, Cynader MS (1988) Transient concordant distributions of nicotinic receptors and acetylcholinesterase activity in infant rat visual cortex. Dev Brain Res 39:154–159
Rakic P (1977) Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc London Ser B 278:245–260
Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176
Rakic P, Goldman-Rakic PS, Gallagher D (1988) Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex. J Neurosci 8:3670–3690
Ramoa AS, Paradiso MA, Freeman RD (1988) Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity. Exp Brain Res 73:285–298
Rasmusson DD (1982) Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J Comp Neurol 205:313–326
Richards RF, Möhler H (1984) Benzodiazepine receptors Neuropharmacology 23:233–242
Shatz CJ, Luskin MB (1986) The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex. J Neurosci 6:3655–3668
Shatz CJ, Chun JJM, Luskin MB (1988) The role of the subplate in the development of the mammalian telencephalon. In: Peters A, Jones EG (eds) The cerebral cortex, Vol 7. Plenum, New York, pp 35–58
Shaw C, Cynader M (1986) Laminar distribution of receptors in monkey (Macaca fascicularis) geniculostriate system. J Comp Neurol 248:301–312
Shaw C, Needler MC, Cynader M (1984) Ontogenesis of muscimol binding sites in cat visual cortex. Brain Res Bull 13:331–334
Sieghart W, Eichinger A, Richards JG, Möhler H (1987) Photoaffinity labeling of benzodiazepine receptor proteins with the partial inverse agonist (3H)Ro15–4513: a biochemical and autoradiographic study. J Neurochem 48:46–52
Sillito AM (1984) Functional considerations of the operation of GABAergic inhibitory processes in the visual cortex. In: Jones EG, Peters A (eds) Cerebral cortex, Vol 2. Plenum, New York, pp 91–117
Somogyi P, Cowey A, Halasz N, Freund TF (1981) Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey. Nature 294:761–763
Somogyi P, Takagi H, Richards JG, Möhler H (1989) Subcellular localization of benzodiazepine/GABAA receptors in the cerebellum of rat, cat and monkey using monoclonal antibodies. J Neurosci 9:2197–2209
Sweetman P, Tallman JF (1986) Regional differences in brain benzodiazepine receptor carbohydrates. Mol Pharmacol 29:299–306
Tallman JF, Thomas JW, Gallager DW (1978) GABAergic modulation of benzodiazepine binding site sensitivity. Nature 274:383–385
Tsumoto T, Eckhart W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res 34:351–363
Valverde F, Facal-Valverde MV (1988) Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: a correlated Golgi and electron microscopic study. J Comp Neurol 269:168–192
Vitorica J, Park D, Chin G, de Blas AL (1988) Monoclonal antibodies and conventional antisera to the GABAA receptor/benzodiazepine/Cl- channel complex. J Neurosci 8:615–622
Wahle P, Meyer G (1987) Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261:165–192
Wall JT, Cusick CG (1984) Cutaneous responsiveness in primary somatosensory (SI) hindpaw cortex before and after partial hindpaw deafferentation in adults rats. J Neurosci 4:1499–1515
Wise SP, Hendry SHC, Jones EG (1977) Prenatal development of sensorimotor cortical projections in cats. Brain Res 138:538–544
Wolff JR (1976) Quantitative analysis of topography and development of synapses in visual cortex. Exp Brain Res Suppl 1:259–263
Woolf NJ, Butcher LL (1981) Cholinergic neurons in the caudateputamen complex proper are intrinsically organized: a combined evans blue and acetylcholinesterase analysis. Brain Res Bull 7:487–507
Wong-Riley MTT (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28
Zecevic N, Bourgeois J-P, Rakic P (1989) Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Dev Brain Res 50:11–32
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Huntley, G.W., de Blas, A.L. & Jones, E.G. GABAA receptor immunoreactivity in adult and developing monkey sensory-motor cortex. Exp Brain Res 82, 519–535 (1990). https://doi.org/10.1007/BF00228794
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228794