Skip to main content
SpringerLink
Log in

Spatial distribution of inhibitory synaptic connections during development of ferret primary visual cortex

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Intracortical inhibition in the primary visual cortex plays an important role in creating properties like orientation and direction selectivity. However, the development of the spatial pattern of inhibitory connections is largely unexplored. This was investigated in the present study. Tangential slices of layers 2/3 of ferret striate cortex were prepared for whole-cell patch clamp recordings, and presynaptic inhibitory inputs to pyramidal neurons were scanned by local photolysis of Nmoc-caged glutamate. Inhibitory synaptic currents (IPSCs) were first detected around postnatal day (P) 17. They originated locally around the recorded cells. Both the number and the total areas supplying the inhibitory inputs increased thereafter and peaked at the time around and shortly after eye opening (P29–37). A refinement period then followed in which the areas providing the majority of inhibitory inputs shrank from 600 µm around the recorded neurons to 200–300 µm in more mature animals (≥P38). The amplitude of IPSCs increased progressively with increasing age. Long-range inhibitory inputs (>600 µm) were present around eye opening and they often developed into a clustered patchy pattern in more mature animals (≥P38). In summary, our results show a refinement and clustering in the spatial pattern of inhibitory connections during postnatal development of ferret visual cortex.

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 A
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12 A

Similar content being viewed by others

References

  • Agmon A, Hollrigel G, O’Dowd DK (1996) Functional GABAergic synaptic connection in neonatal mouse barrel cortex. J Neurosci 16:4684–4695

    CAS  PubMed  Google Scholar 

  • Albus K, Wahle P (1994) The topography of tangential inhibitory connections in the postnatally developing and mature striate cortex of the cat. Eur J Neurosci 6:779–792

    CAS  PubMed  Google Scholar 

  • Albus K, Wahle P, Lubke J, Matute C (1991) The contribution of GABA-ergic neurons to horizontal intrinsic connections in upper layers of the cat’s striate cortex. Exp Brain Res 85:235–239

    Article  CAS  PubMed  Google Scholar 

  • Allison JD, Kabara JF, Snider RK, Casagrande VA, Bonds AB (1996) GABAB-receptor-mediated inhibition reduces the orientation selectivity of the sustained response of striate cortical neurons in cats. Vis Neurosci 13:559–566

    CAS  PubMed  Google Scholar 

  • Azouz R, Gray CM, Nowak LG, McCormick DA (1997) Physiological properties of inhibitory interneurons in cat striate cortex. Cereb Cortex 7:534–545

    Article  CAS  PubMed  Google Scholar 

  • Beaulieu C, Somogyi P (1990) Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur J Neurosci 2:296–303

    PubMed  Google Scholar 

  • Berman NJ, Douglas RJ, Martin KA, Whitteridge D (1991) Mechanisms of inhibition in cat visual cortex. J Physiol 440:667–722

    Google Scholar 

  • Berman NJ, Douglas RJ, Martin KAC (1992) GABA-mediated inhibition in the neural networks of visual cortex. Prog Brain Res 90:443–476

    CAS  PubMed  Google Scholar 

  • Blakemore C, Van Sluyters RC (1975) Innate and environmental factors in the development of kitten’s visual cortex. J Physiol 248:663–716

    CAS  PubMed  Google Scholar 

  • Blue ME, Parnavelas JG (1983) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol 12:697–712

    CAS  PubMed  Google Scholar 

  • Bonhoeffer T, Grinvald A (1991) Iso-orientation domains in cat visual cortex are arranged in pinwheel like patterns. Nature 353:429–431

    Article  CAS  PubMed  Google Scholar 

  • Buisseret P, Imbert M (1976) Cortical cells: their developmental properties in normal and dark reared kittens. J Physiol 255:511–525

    CAS  PubMed  Google Scholar 

  • Callaway EM, Katz LC (1990) Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurosci 10:1134–1153

    CAS  PubMed  Google Scholar 

  • Callaway EM, Katz LC (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci U S A 90:7661–7665

    CAS  PubMed  Google Scholar 

  • Chapman B, Stryker MP (1992) Origin of orientation tuning in the visual cortex. Curr Opin Neurobiol 2:498–501

    Article  CAS  PubMed  Google Scholar 

  • Chapman B, Stryker MP (1993) Development of orientation selectivity in ferret visual cortex and effects of deprivation. J Neurosci 13:5251–5262

    CAS  PubMed  Google Scholar 

  • Chapman B, Stryker MP, Bonhoeffer T (1996) Development of orientation preference maps in ferret primary visual cortex. J Neurosci 16:6443–6453

    CAS  PubMed  Google Scholar 

  • Crook JM, Eysel UT, Machemer HF (1991) Influence of GABA-induced remote inactivation on the orientation tuning of cells in area 18 of feline visual cortex: a comparison with area 17. Neuroscience 40:1–12

    Article  CAS  PubMed  Google Scholar 

  • Crook JM, Kisvarday ZF, Eysel UT (1997) GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity. Vis Neurosci 14:141–158

    CAS  PubMed  Google Scholar 

  • Dalva MB, Katz LC (1994) Rearrangements of synaptic connections in visual cortex revealed by laser photostimulation. Science 265:255–258

    CAS  PubMed  Google Scholar 

  • Dalva MB, Weliky M, Katz LC (1997) Relationships between local synaptic connections and orientation domains in primary visual cortex. Neuron 19:871–880

    Article  CAS  PubMed  Google Scholar 

  • Dantzker JL, Callaway EM (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701–7

    Article  CAS  PubMed  Google Scholar 

  • Eysel UT (1992) Lateral inhibitory interactions in areas 17 and 18 of the cat visual cortex. Prog Brain Res 90:407–422

    CAS  PubMed  Google Scholar 

  • Eysel UT, Muche T, Worgotter F (1988) Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation. J Physiol 399:657–675

    CAS  PubMed  Google Scholar 

  • Eysel UT, Crook JM, Machemer HF (1990) GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Exp Brain Res 80:626–630

    Article  CAS  PubMed  Google Scholar 

  • Ferster D, Chung S, Wheat HS (1996) Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380:249–252

    Article  CAS  PubMed  Google Scholar 

  • Gao WJ, Newman DE, Wormington AB, Pallas SL (1999) Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of GABAergic neurons. J Comp Neurol 409:261–273

    Article  CAS  PubMed  Google Scholar 

  • Gibber M, Chen B, Roerig B (2001) Direction selectivity of excitatory and inhibitory neurons in ferret visual cortex. Neuroreport 12:2293–2296

    Article  CAS  PubMed  Google Scholar 

  • Goedecke I, Bonhoeffer T (1996) Development of identical orientation maps for two eyes without common visual experience. Nature 379:251–254

    Article  CAS  PubMed  Google Scholar 

  • Heggelund P (1981) Receptive field organization of simple cells in cat striate cortex. Exp Brain Res 42:89–98

    CAS  PubMed  Google Scholar 

  • Heinen K, Bosman LW, Spijker S, Van Pelt J, Smit AB, Voorn P, Baker RE, Brussaard AB (2004) GABA(a) receptor maturation in relation to eye opening in the rat visual cortex. Neuroscience124:161–171

  • Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504–1508

    Article  CAS  PubMed  Google Scholar 

  • Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739–755

    Article  CAS  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1962) Receptive fields, binocular interactions and functional architecture in the cat’s visual cortex. J. Physiol (Lond) 160:106–154

    Google Scholar 

  • Hubel DH, Wiesel TN (1963) Shape and arrangement of columns in cat’s striate cortex. J. Physiol (Lond) 165:559–568

    Google Scholar 

  • Katz LC, Dalva MB (1994) Scanning photostimulation: a new approach for analyzing brain circuits. J Neurosci Methods 54:205–218

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 6:476–486

    Article  Google Scholar 

  • Kim G, Kandler K (2003) Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6:282–290

    Article  CAS  PubMed  Google Scholar 

  • Kirkwood A, Bear MF (1994) Hebbian synapses in visual cortex. J Neurosci 14:1634–1635

    CAS  PubMed  Google Scholar 

  • Kirkwood A, Silva A, Bear MF (1997) Age-dependent decrease of synaptic plasticity in the neocortex of αCaMkII mutant mice. Proc Natl Acad Sci U S A 94:3380–3383

    Article  CAS  PubMed  Google Scholar 

  • Kisvarday ZF (1992) GABAergic networks of basket cells in the visual cortex. Prog Brain Res 90:385–405

    CAS  PubMed  Google Scholar 

  • Kisvarday ZF, Beaulieu C, Eysel UT (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327:398–415

    CAS  PubMed  Google Scholar 

  • Komatsu Y, Iwakiri M (1991) Postnatal development of neuronal connections in cat visual cortex studied by intracellular recording in slice preparation. Brain Res 540:14–24

    Article  CAS  PubMed  Google Scholar 

  • Kritzer MF, Cowey A, Somogyi P (1992) Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices: their functionally specialized subdivisions in the rhesus monkey. J Neurosci 12:4545–4564

    CAS  PubMed  Google Scholar 

  • Lubke J, Albus K (1992) Rapid rearrangement of intrinsic tangential connections in the striate cortex of normal and dark-reared kittens: lack of exuberance beyond the second postnatal week. J Comp Neurol 323:42–58

    CAS  PubMed  Google Scholar 

  • Luhmann HJ, Prince DA (1991) Postnatal maturation of GABAergic system in rat neocortex. J Neurophysiol 65:247–263

    CAS  PubMed  Google Scholar 

  • Luskin MB, Shatz CJ (1985) Neurogenesis of the cat’s primary visual cortex. J Comp Neurol 242:611–631

    CAS  PubMed  Google Scholar 

  • Martin KAC (1988) From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol 73:637–702

    CAS  PubMed  Google Scholar 

  • Micheva KD, Beaulieu C (1997) Development and plasticity of the inhibitory neocortical circuitry with an emphasis on the rodent barrel field cortex: a review. Can J Physiol Pharmacol 75:470–478

    Article  CAS  PubMed  Google Scholar 

  • Miller MW (1986) The migration and neurochemical differentiation of gamma-aminobutyric acid (GABA)-immunoreactive neurons in rat visual cortex as demonstrated by a combined immunocytochemical–autoradiographic technique. Brain Res 1:41–46

    Article  Google Scholar 

  • Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF (1999) Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397:347–350

    Article  CAS  PubMed  Google Scholar 

  • Rockland KS. Lund JS. Humphrey AL (1982) Anatomical binding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). J Comp Neurol 209:41–58

    CAS  PubMed  Google Scholar 

  • Roerig B, Chen B (2002) Relationships of local inhibitory and excitatory circuits to orientation preference maps in ferret visual cortex. Cereb Cortex 12:187–198

    Article  CAS  PubMed  Google Scholar 

  • Roerig B, Kao JP (1999) Organization of intracortical circuits in relation to direction preference maps in ferret visual cortex. J Neurosci 1999 19(24):RC44

    CAS  Google Scholar 

  • Rossi FM, Margulis M, Tang CM, Kao JP (1997) N-Nmoc-L-glutamate, a new caged glutamate with high chemical stability and low pre-photolysis activity. J Biol Chem 272:32933–32939

    Article  CAS  PubMed  Google Scholar 

  • Sanes DH, Takacs C (2003) Activity-dependent refinement of inhibitory connections. Eur J Neurosci 6:570–574

    Google Scholar 

  • Sawatari A, Callaway EM (2000) Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex. Neuron 2:459–471

    Article  Google Scholar 

  • Shepherd GM, Pologruto TA, Svoboda K (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277–298

    Article  CAS  PubMed  Google Scholar 

  • Shmuel A, Grinvald A (1996) Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J Neurosci 16:6945–6964

    CAS  PubMed  Google Scholar 

  • Sillito AM (1979) Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol 289:33–53

    CAS  PubMed  Google Scholar 

  • 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 Press, New York, pp 91–117

  • Sillito AM, Kemp JA, Milson JA, Berardi N (1980) A reevaluation of the mechanisms underlying simple cell organization selectivity. Brain Res 194:517–520

    Article  CAS  PubMed  Google Scholar 

  • Somers DC, Nelson SB, Sur M (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci 15:5448–5465

    CAS  PubMed  Google Scholar 

  • Vidyasagar TR, Pei X, Volgushev M (1996) Multiple mechanisms underlying the orientation selectivity of visual cortical neurons. Trends Neurosci 19:272–277

    Article  CAS  PubMed  Google Scholar 

  • Weliky M, Bosking WH, Fitzpatrick D (1996) A systematic map of direction preference in primary visual cortex. Nature 379:725–728

    Article  CAS  PubMed  Google Scholar 

  • Winfield DA. The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. Brain Res 285:155–169

  • Woergoetter F, Koch C (1991) A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. J Neurosci 11:1959–1979

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, University of Maryland at Baltimore, 685 West Baltimore Street, Baltimore, MD 21201-1509, USA

    Bingzhong Chen, Kaoutar Boukamel & Birgit Roerig

  2. Medical Biotechnology Center and Department of Physiology, University of Maryland at Baltimore, School of Medicine, Baltimore, Maryland, USA

    Joseph P.-Y. Kao

Authors
  1. Bingzhong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaoutar Boukamel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph P.-Y. Kao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Birgit Roerig
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bingzhong Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, B., Boukamel, K., Kao, J.PY. et al. Spatial distribution of inhibitory synaptic connections during development of ferret primary visual cortex. Exp Brain Res 160, 496–509 (2005). https://doi.org/10.1007/s00221-004-2029-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-004-2029-4

Keywords

Search

Navigation