Elsevier

Neuroscience

Volume 102, Issue 1, 2 January 2001, Pages 35-52
Neuroscience

Intra- and inter-areal connections between the primary visual cortex V1 and the area immediately surrounding V1 in the rat

https://doi.org/10.1016/S0306-4522(00)00475-9Get rights and content

Abstract

We have qualitatively and quantitatively analysed the anatomical connections within and between rat primary visual cortex (V1) and the rim region surrounding area V1, using both ortho- and retrograde anatomical tracers (biotinylated dextran amine, biocytin, cholera toxin b subunit). From the analysis of the projection patterns, and with the assumption that single points in the rat visual cortex, as in other species, have projection fields made up of multiple patches of terminals, we have concluded that just two V1 recipient areas occupy the entire rim region: an anterolateral area, probably homologous with V2 in other mammals, previously named Oc2L, and a medial area, corresponding to Oc2M. A non-reciprocal projection from the anterolateral area to the medial area was identified.

Small injections (300–600 μm uptake zone diameter) of the anatomical tracers in area V1, or in the rim region, label orthograde intra-areal connections from each injection site to offset small patches. This is found in all regions of the rim and within at least the relatively expanded central dorsal field representation of V1. From the extent of these projections in V1 and the two rim regions, we have estimated that the neurons at the injection site send diverging laterally spreading projections to other neurons whose receptive fields share any part of the area included in the pooled receptive fields of the neurons at the injection site. Orthogradely labelled inter-areal feedforward projections from V1 to either rim region are estimated to diverge in their projections to neurons that share any part of the area of the pooled receptive fields of the V1 intra-areal connectional field of the same injection. The orthogradely labelled feedback projections to V1, from injection sites in either rim region, reach V1 neurons whose pooled receptive fields match those of the neurons in the rim injection site, i.e. with no divergence.

Despite patchy anatomical connectional fields, our estimates indicate that visual space is represented continuously in the receptive fields of neurons postsynaptic to each intra- or inter-areal field of orthograde label. We suggest that, despite the absence of regularly mapped functions in rat V1 (e.g. regularly arranged orientation specificity), which in other species (e.g. primates and cats) relate to the patchy connectional patterns, the rat visual cortex intra- and inter-areal anatomical connections follow similar patterns and scaling factors to those in other species.

Section snippets

Animals and injection procedures

Out of a larger sample, a total of 17 rats (female Long–Evans Hooded, weight 150 g) were included in this study, in two series of experiments. Anaesthesia was induced with 3% Halothane in a small anaesthetic chamber, and maintained with intraperitoneal injection of a 2.7 mg/kg solution of fentanyl citrate and fluanisone (Hypnorm: 0.315 mg/ml fentanyl citrate, 10 mg/ml fluanisone; Janssen-Cilag) and midazolam (Hypnovel: 5 mg/ml; Roche). Single small injections of anatomical tracer were made in area

General observations

As observed previously,67 V1 can be distinguished from its surrounding rim region by its denser myelin staining. In our myelin-stained material, V1 was estimated to have a 7–8 mm2 area (our estimate of shrinkage compared to the in vivo state is slightly more than 10% along one axis); the total area of the V1 recipient rim territory was about 7 mm2. These values correspond to published figures14 of 7 mm2 for V1 and 6 mm2 for the V1 recipient rim region. In the rim region, we found the medial area (

Technical considerations

In the course of these anatomical experiments, it was clear that the three anatomical tracers used each transported with different emphasis on retro- and orthograde directions. The orthograde labelling with BDA and biocytin was very comparable, producing in all cases clear distinction between a local zone of fibre and terminal staining immediately surrounding the injection site, and patches of terminal label offset from this local label and separated from it by terminal sparse regions. The

Conclusion

This study has emphasized commonalties that could exist between the rat and other animals in terms of scaling and patterning of intra-areal, feedforward and feedback pathways. We suggest that the difficulty in obtaining agreement between investigators exploring rat visual cortex retinotopic maps and in definition of boundaries in the rim region using physiological recording techniques could be due to patchy systems of feedforward, feedback and intra-areal connections. Such connectivity may

Acknowledgements

We would like to thank Drs A. Angelucci and R. Lund for comments on the manuscript, and S. Griffiths for photographic help and K. Sainsbury for expert technical assistance. The work was supported by MRC grant G9408137.

References (67)

  • Angelucci A., Levitt J. B., Hupé J. M., Walton E., Bullier J. and Lund J. S. (2000) Anatomical circuits for local and...
  • G.G Blasdel et al.

    Voltage-sensitive dyes reveal a modular organisation in the monkey striate cortex

    Nature

    (1986)
  • G.G Blasdel et al.

    Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C

    J. Neurosci.

    (1985)
  • W.H Bosking et al.

    Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex

    J. Neurosci.

    (1997)
  • A Burkhalter

    Intrinsic connections of rat primary visual cortex: laminar organisation of axonal projections

    J. comp. Neurol.

    (1989)
  • V.S Caviness

    Architectonic map of the neocortex of the normal mouse

    J. comp. Neurol.

    (1975)
  • Chalupa L. M. (1984) Visual physiology of the mammalian superior colliculus. In Comparative Neurology of the Optic...
  • T.A Coogan et al.

    Conserved patterns of cortico-cortical connections define areal hierarchy in rat visual cortex

    Expl Brain Res.

    (1990)
  • T.A Coogan et al.

    Hierarchical organisation of areas in rat visual cortex

    J. Neurosci.

    (1993)
  • U.C Dräger

    Receptive fields of single cells and topography in mouse visual cortex

    J. comp. Neurol.

    (1975)
  • D.J Felleman et al.

    Distributed hierarchical processing in the primate cerebral cortex

    Cerebral Cortex

    (1991)
  • S.V Girman et al.

    Receptive field properties of single neurons in rat primary visual cortex

    J. Neurophysiol.

    (1999)
  • A.R Harvey et al.

    The projection from different visual cortical areas to the rat superior colliculus

    J. comp. Neurol.

    (1990)
  • D.H Hubel et al.

    Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex

    J. Physiol., Lond.

    (1962)
  • D.H Hubel et al.

    Sequence regularity and geometry of orientation columns in the monkey striate cortex

    J. comp. Neurol.

    (1974)
  • Huerta M. F. and Harting J. K. (1984) The mammalian superior colliculus: studies of its morphology and its connections....
  • A.L Humphrey et al.

    Topographic organisation of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). I. Microelectrode recording

    J. comp. Neurol.

    (1980)
  • A.L Humphrey et al.

    Topographic organisation of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping

    J. comp. Neurol.

    (1980)
  • G.M Innocenti et al.

    The organisation of immature callosal connections

    J. comp. Neurol.

    (1984)
  • J.H Kaas et al.

    Cortical connections of areas 17 (V-I) and 18 (V-II) of squirrels

    J. comp. Neurol.

    (1989)
  • A Larkman et al.

    Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes

    J. Neurosci.

    (1990)
  • M.I Law et al.

    Organisation of primary visual cortex (area 17) in the ferret

    J. comp. Neurol.

    (1988)
  • J.B Levitt et al.

    Intrinsic cortical connections in macaque visual area V2: evidence for interaction between different functional streams

    J. comp. Neurol.

    (1994)
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    Present address: Department of Physiology, New York Medical College, New York, NY 10595, USA.

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