Skip to main content
SpringerLink
Log in

Laminar distribution and co-distribution of neurotransmitter receptors in early human visual cortex

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The laminar distributions of 16 neurotransmitter receptor binding sites were analysed in visual cortical areas V1–V3 by quantitative in vitro receptor autoradiography. For each receptor (glutamatergic: AMPA, kainate, NMDA; cholinergic: M1, M2, M3, nicotinic; GABAergic: GABAA, GABAB, benzodiazepine binding-sites; adrenergic: α1, α2; serotoninergic: 5-HT1A, 5-HT2; dopaminergic: D1; Adenosine: A1), density profiles extracted perpendicular to the cortical surface were compared to cyto- and myeloarchitectonic profiles sampled at corresponding cortical sites. When testing for differences in laminar distribution patterns, all receptor-density profiles differed significantly from the cyto- and myeloarchitectonic ones. These results indicate that receptor distribution is an independent feature of the cortical architecture not predictable by densities of cell bodies or myelinated fibres. Receptor co-distribution was studied by cluster analyses, revealing several groups of receptors, which showed similar laminar distribution patterns across all analysed areas (V1–V3). Other receptors were co-distributed in extrastriate but not primary visual cortex. Finally, some receptors were not co-distributed with any of the analysed other ones. A comparison of the laminar patterns of receptor binding sites in the human visual cortex with those reported for non-human primates and other mammals showed that the laminar distributions of cholinergic and glutamatergic receptors seem largely preserved, while serotoninergic and adrenergic receptors appear to be more variable between different species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Albin RL, Sakurai SY, Makowiec RL, Higgins DS, Young AB, Penney JB (1991) Excitatory amino acid, GABA(A), and GABA(B) binding sites in human striate cortex. Cerebr Cortex 1:499–509

    Article  CAS  Google Scholar 

  • Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HB, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341

    Article  PubMed  CAS  Google Scholar 

  • Carlson MD, Penney JB Jr, Young AB (1993) NMDA, AMPA, and benzodiazepine binding site changes in Alzheimer’s disease visual cortex. Neurobiol Aging 14:343–352

    Article  PubMed  CAS  Google Scholar 

  • Eickhoff SB, Schleicher A, Scheperjans F, Palomero-Gallagher N, Zilles K (2007) Analysis of neurotransmitter receptor distribution patterns in the cerebral cortex. Neuroimage 34(4):1317–1330

    Article  PubMed  Google Scholar 

  • Friston KJ, Frith CD, Fletcher P, Liddle PF, Frackowiak RS (1996) Functional topography: multidimensional scaling and functional connectivity in the brain. Cerebr Cortex 6:156–164

    Article  CAS  Google Scholar 

  • Friston KJ, Holmes AP, Price CJ, Buchel C, Worsley KJ (1999) Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385–396

    Article  PubMed  CAS  Google Scholar 

  • Gebhard R, Zilles K, Schleicher A, Everitt BJ, Robbins TW, Divac I, (1993) Distribution of seven major neurotransmitter receptors in the striate cortex of the New World monkey Callithrix jacchus. Neuroscience 56:877–885

    Article  PubMed  CAS  Google Scholar 

  • Gordon B, Kinch G, Kato N, Keele C, Lissman T, Fu LN (1997) Development of MK-801, kainate, AMPA, and muscimol binding sites and the effect of dark rearing in rat visual cortex. J Comp Neurol 383:73–81

    Article  PubMed  CAS  Google Scholar 

  • Gordon B, Pardo D, Conant K (1996) Laminar distribution of MK-801, kainate, AMPA, and muscimol binding sites in cat visual cortex: a developmental study. J Comp Neurol 365:466–478

    Article  PubMed  CAS  Google Scholar 

  • Gu Q (2003) Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 80:291–301

    Article  PubMed  CAS  Google Scholar 

  • Han ZY, Zoli M, Cardona A, Bourgeois JP, Changeux JP, Le NN (2003) Localization of [3H]nicotine, [3H]cytisine, [3H]epibatidine, and [125I]alpha-bungarotoxin binding sites in the brain of Macaca mulatta. J Comp Neurol 461:49–60

    Article  PubMed  CAS  Google Scholar 

  • Hendry S, Carder RK (1992) Organization and plasticity of GABA neurons and receptors in monkey visual cortex. Prog Brain Res 90:477–502

    PubMed  CAS  Google Scholar 

  • Hendry SH, Fuchs J, deBlas AL, Jones EG (1990) Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J Neurosci 10:2438–2450

    PubMed  CAS  Google Scholar 

  • Hendry SH, Huntsman MM, Vinuela A, Mohler H, de Blas AL, Jones EG (1994) GABAA receptor subunit immunoreactivity in primate visual cortex: distribution in macaques and humans and regulation by visual input in adulthood. J Neurosci 14:2383–2401

    PubMed  CAS  Google Scholar 

  • Huntley GW, Vickers JC, Janssen W, Brose N, Heinemann SF, Morrison JH (1994) Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor and visual cortices of monkey and human. J Neurosci 14:3603–3619

    PubMed  CAS  Google Scholar 

  • Kaas JH (1996) Theories of visual cortex organization in primates: areas of the third level. Prog Brain Res 112:213–221

    Article  PubMed  CAS  Google Scholar 

  • Kaas JH, Lyon DC (2001) Visual cortex organization in primates: theories of V3 and adjoining visual areas. Prog Brain Res 134:285–295

    PubMed  CAS  Google Scholar 

  • Kew JN, Kemp JA (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacol (Berl) 179:4–29

    Article  CAS  Google Scholar 

  • Kontur PJ, al Tikriti M, Innis RB, Roth RH (1994) Postmortem stability of monoamines, their metabolites, and receptor binding in rat brain regions. J Neurochem 62:282–290

    Article  PubMed  CAS  Google Scholar 

  • Kosofsky BE, Molliver ME, Morrison JH, Foote SL (1984) The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 230:168–178

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Schliebs R (1993) Postnatal ontogeny of GABAA and benzodiazepine receptors in individual layers of rat visual cortex and the effect of visual deprivation. Neurochem Int 23:99–106

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Schliebs R, Bigl V (1994) Postnatal development of NMDA, AMPA, and kainate receptors in individual layers of rat visual cortex and the effect of monocular deprivation. Int J Dev Neurosci 12:31–41

    Article  PubMed  CAS  Google Scholar 

  • Lidow MS, Gallager DW, Rakic P, Goldman-Rakic PS (1989) Regional differences in the distribution of muscarinic cholinergic receptors in the macaque cerebral cortex. J Comp Neurol 289:247–259

    Article  PubMed  CAS  Google Scholar 

  • Mash DC, White WF, Mesulam MM (1988) Distribution of muscarinic receptor subtypes within architectonic subregions of the primate cerebral cortex. J Comp Neurol 278:265–274

    Article  PubMed  CAS  Google Scholar 

  • Morosan P, Schleicher A, Amunts K, Zilles K (2005) Multimodal Architectonic Mapping of Human Superior Temporal Gyrus. Anat Embryol (Berl) 210(5–6):401–406

    Article  CAS  Google Scholar 

  • Morrison JH, Foote SL, O’Connor D, Bloom FE (1982) Laminar, tangential and regional organization of the noradrenergic innervation of monkey cortex: dopamine-beta-hydroxylase immunohistochemistry. Brain Res Bull 9:309–319

    Article  PubMed  CAS  Google Scholar 

  • Parkinson D, Coscia EC, Daw NW (1989) Identification and localization of 5-hydroxytryptamine receptor sites in macaque visual cortex. Vis Neurosci 2:515–525

    Article  PubMed  CAS  Google Scholar 

  • Power AE, Vazdarjanova A, McGaugh JL (2003) Muscarinic cholinergic influences in memory consolidation. Neurobiol Learn Mem 80:178–193

    Article  PubMed  CAS  Google Scholar 

  • Prusky GT, Shaw C, Cynader MS (1988) The distribution and ontogenesis of [3H]nicotine binding sites in cat visual cortex. Brain Res 467:161–176

    PubMed  CAS  Google Scholar 

  • Rakic P, Goldman-Rakic PS, Gallager D (1988) Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex. J Neurosci 8:3670–3690

    PubMed  CAS  Google Scholar 

  • Rakic P, Lidow MS (1995) Distribution and density of monoamine receptors in the primate visual cortex devoid of retinal input from early embryonic stages. J Neurosci 15:2561–2574

    PubMed  CAS  Google Scholar 

  • Rosa MG, Manger PR (2005) Clarifying homologies in the mammalian cerebral cortex: the case of the third visual area (V3). Clin Exp Pharmacol Physiol 32:327–339

    Article  PubMed  CAS  Google Scholar 

  • Rosier AM, Arckens L, Demeulemeester H, Orban GA, Eysel UT, Wu YJ, Vandesande F (1995) Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex. J Comp Neurol 359:476–489

    Article  PubMed  CAS  Google Scholar 

  • Rosier AM, Arckens L, Orban GA, Vandesande F (1993) Laminar distribution of NMDA receptors in cat and monkey visual cortex visualized by [3H]-MK-801 binding. J Comp Neurol 335:369–380

    Article  PubMed  CAS  Google Scholar 

  • Rottschy C, Eickhoff SB, Schleicher A, Mohlberg H, Kujovic M, Zilles K, Amunts K (2007) The ventral visual cortex in humans: cytoarchitectonic mapping of two extrastriate areas. Hum Brain Map (doi:10.1002/hbm.20348 )

  • Scheperjans F, Grefkes C, Palomero-Gallagher N, Schleicher A, Zilles K (2005a) Subdivisions of human parietal area 5 revealed by quantitative receptor autoradiography: a parietal region between motor, somatosensory, and cingulate cortical areas. Neuroimage 25:975–992

    Article  PubMed  Google Scholar 

  • Scheperjans F, Palomero-Gallagher N, Grefkes C, Schleicher A, Zilles K (2005b) Transmitter receptors reveal segregation of cortical areas in the human superior parietal cortex: relations to visual and somatosensory regions. Neuroimage 28(2):362–379

    Article  PubMed  Google Scholar 

  • Schleicher A, Palomero-Gallagher N, Morosan P, Eickhoff SB, Kowalski T, de Vos K, Amunts K, Zilles K (2005) Quantitative architectectural analysis: a new approach to cortical mapping. Anat Embryol (Berl) 210:373–386

    Article  CAS  Google Scholar 

  • Schliebs R, Rossner S, Kumar A, Bigl V (1994) Muscarinic acetylcholine receptor subtypes in rat visual cortex–a comparative study using quantitative receptor autoradiography and in situ hybridization. Indian J Exp Biol 32:25–30

    PubMed  CAS  Google Scholar 

  • Schliebs R, Walch C, Stewart MG (1989) Laminar pattern of cholinergic and adrenergic receptors in rat visual cortex using quantitative receptor autoradiography. J Hirnforsch 30:303–311

    PubMed  CAS  Google Scholar 

  • Shaw C, Cameron L, March D, Cynader M, Zielinski B, Hendrickson A (1991) Pre- and postnatal development of GABA receptors in Macaca monkey visual cortex. J Neurosci 11:3943–3959

    PubMed  CAS  Google Scholar 

  • Smith AL, Thompson ID (1994) Distinct laminar differences in the distribution of excitatory amino acid receptors in adult ferret primary visual cortex. Neuroscience 61:467–479

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Sano Y (1984) Serotonin nerve fibers in the primary visual cortex of the monkey. Quantitative and immunoelectronmicroscopical analysis. Anat Embryol (Berl) 169:1–8

    Article  CAS  Google Scholar 

  • Tigges M, Tigges J, Rees H, Rye D, Levey AI (1997) Distribution of muscarinic cholinergic receptor proteins m1 to m4 in area 17 of normal and monocularly deprived rhesus monkeys. J Comp Neurol 388:130–145

    Article  PubMed  CAS  Google Scholar 

  • Timm NH (2002) Applied multivariate analysis. Springer, New York

    Google Scholar 

  • Yi BA, Minor DL Jr, Lin YF, Jan YN, Jan LY (2001) Controlling potassium channel activities: Interplay between the membrane and intracellular factors. Proc Natl Acad Sci USA 98:11016–11023

    Article  PubMed  CAS  Google Scholar 

  • Zilles K (1991) Codistribution of receptors in the human cerebral cortex. In: Mendelsohn FAO, Paxinos GE (Eds) Receptors in the human nervous system. Academic, San Diego, pp 165–206

    Google Scholar 

  • Zilles K, Eickhoff S, Palomero-Gallagher N (2003) The human parietal cortex: a novel approach to its architectonic mapping. Adv Neurol 93:1–21

    PubMed  Google Scholar 

  • Zilles K, Palomero-Gallagher N, Grefkes C, Scheperjans F, Boy C, Amunts K, Schleicher A (2002a) Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry. Eur Neuropsychopharmacol 12:587–599

    Article  PubMed  CAS  Google Scholar 

  • Zilles K, Palomero-Gallagher N, Schleicher A (2004) Transmitter receptors and functional anatomy of the cerebral cortex. J Anat 205:417–432

    Article  PubMed  CAS  Google Scholar 

  • Zilles K, Schlaug G, Geyer S, Luppino G, Matelli M, Qu M, Schleicher A, Schormann T (1996) Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. Adv Neurol 70:29–43

    PubMed  CAS  Google Scholar 

  • Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002b) Quantitative analysis of cyto- and receptor architecture of the human brain. In: Mazziotta J, Toga A (eds) Brain mapping, the methods. Elsevier, Amsterdam, pp 573–602

    Google Scholar 

  • Zinke W, Roberts MJ, Guo K, McDonald JS, Robertson R, Thiele A (2006) Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized Marmoset monkeys. Eur J Neurosci 24:314–328

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This Human Brain Project/Neuroinformatics research is funded by the National Institute of Biomedical Imaging and Bioengineering, the National Institute of Neurological Disorders and Stroke, and the National Institute of Mental Health and the Deutsche Forschungsgemeinschaft (KFO-112).

Author information

Authors and Affiliations

  1. Institut für Medizin (IME), Forschungszentrum Jülich GmbH, 52425, Jülich, Germany

    Simon B. Eickhoff, Claudia Rottschy & Karl Zilles

  2. C. & O. Vogt Institut für Hirnforschung, Düsseldorf, Germany

    Simon B. Eickhoff, Claudia Rottschy & Karl Zilles

  3. Brain Imaging Center West (BICW), Jülich, Germany

    Karl Zilles

Authors
  1. Simon B. Eickhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Rottschy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karl Zilles
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simon B. Eickhoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eickhoff, S.B., Rottschy, C. & Zilles, K. Laminar distribution and co-distribution of neurotransmitter receptors in early human visual cortex. Brain Struct Funct 212, 255–267 (2007). https://doi.org/10.1007/s00429-007-0156-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-007-0156-y

Keywords

Search

Navigation