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Quantitative analyses of principal and secondary compound parieto-occipital feedback pathways in cat

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Abstract

The purpose of our study was to quantify the magnitude of principal and secondary pathways emanating from the middle suprasylvian (MS) region of visuoparietal cortex and terminating in area 18 of primary visual cortex. These pathways transmit feedback signals from visuoparietal cortex to primary visual cortex. (1) WGA-HRP was injected into area 18 to identify inputs from visual structures. In terms of numbers of neurons, feedback projections to area 18 from MS sulcal cortex (areas PMLS, AMLS and PLLS) comprise 26% of inputs from all visual structures. Of these neurons, between 21% and 34.9% are located in upper layers 2–4 and the dominant numbers are located in deep layers 5 and 6. Areas 17 (11.8%) and 19 (11.2%) provide more modest cortical inputs, and another eight areas provide a combined total of 4.3% of inputs. The sum of neurons in all subcompartments of the lateral geniculate nucleus (LGN) accounts for another 34.8% of the input to area 18, whereas inputs from the lateral division of the lateral-posterior nucleus (LPl) account for the final 11.9%. (2) Injection of tritiated-(3H)-amino acids into MS sulcal cortex revealed substantial direct projections from MS cortex that terminated in all layers of area 18, but with a markedly lower density in layer 4. Projections from MS cortex to both areas 17 and 19 are of similar density and characteristics, whereas those to other cortical targets have very low densities. Quantification also revealed minor-to-modest axon projections to all components of LGN and a massive projection throughout the LP-Pul complex. (3) Superposition of the labeled terminal and cell fields identified secondary, compound feedback pathways from MS cortex to area 18. The largest secondary pathway is massive and it includes the LPl nucleus. Much more modest secondary pathways include areas 17 and 19, and LGN. The relative magnitudes of the secondary pathways suggest that the one through LPl exerts a major influence on area 18, whereas the others exert more modest or minor influences. MS cortex in the contralateral hemisphere also innervates area 18 directly. These data are important for interpreting the impact of deactivating feedback projections from visuoparietal cortex on occipital cortex.

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Abbreviations

A:

layer A of LGN

A1:

layer A1 of LGN

ALLS:

anterolateral visual area of the lateral suprasylvian sulcus (Palmer et al. 1978)

AMLS:

anteromedial visual area of the lateral suprasylvian sulcus (Palmer et al. 1978)

Aud:

auditory cortex of the middle ectosylvian gyrus

CC:

corpus callosum

Cg:

cingulate gyrus

Cm:

magnocellular layers of LGN

Cp:

parvocellular layers of LGN

LGN:

dorsal lateral geniculate nucleus

LP:

lateral posterior nucleus

LPl:

lateral division of the lateral posterior nucleus

LPm:

medial division of the lateral posterior nucleus (Graybiel and Berson 1980, Berson and Graybiel 1978; Raczkowski and Rosenquist 1983)

MIN:

medial interlaminar nucleus subdivision of LGN

MS:

cortex bounding the middle suprasylvian sulcus (areas AMLS, ALLS, PMLS, and PLLS)

OR:

optic radiation

PE:

posterior ectosylvian visual cortex

PLLS:

posterolateral visual area of the lateral suprasylvian sulcus (Palmer et al. 1978)

PMLS:

posteromedial visual area of the lateral suprasylvian sulcus (Palmer et al. 1978)

Pul:

pulvinar nucleus

SVA:

splenial visual area

V1:

primary visual cortex

V2:

secondary visual cortex

V3:

third visual area

V5/MT:

fifth visual area/middle temporal area

WGA-HRP:

wheat germ agglutinin conjugated to horseradish peroxidase

Wing:

wing of LGN

7:

area 7

17:

area 17

18:

area 18

19:

area 19

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Acknowledgements

We would like to thank the National Institute of Neurological Diseases and Stroke for financial support and Jarrett Rushmore, Ralf Galuske, Kerstin Schmidt, Julian Budd and an anonymous reviewer for their comments. We also thank Dr. Wolf Singer for hosting BRP at the Max-Planck Institute for Brain Research, Frankfurt, Germany, for the preparation of much of the manuscript. Financial support of DAAD for travel to Frankfurt is gratefully acknowledged.

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  1. Cerebral Dynamics, Center for Advanced Biomedical Research, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118, USA

    Bertram R. Payne

  2. Cerebral Systems Laboratory, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX 75083-0688, USA

    Stephen G. Lomber

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Payne, B.R., Lomber, S.G. Quantitative analyses of principal and secondary compound parieto-occipital feedback pathways in cat. Exp Brain Res 152, 420–433 (2003). https://doi.org/10.1007/s00221-003-1554-x

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