Efferent systems of the rabbit visual cortex: Laminar distribution of the cells of origin, axonal conduction velocities, and identification of axonal branches

Several efferent systems of visual area I in Dutch rabbits were studied with anatomical (horseradish peroxidase) and physiological (antidromic) methods. Anatomical studies provided information regarding the laminar origin of the projections to the contralateral hemisphere, visual area II, the dorsal lateral geniculate nucleus, and the superior colliculus. Physiological studies provided information regarding conduction velocities and multiple destinations of efferent axons. Both the callosal projection and the projection to V‐II were shown to originate primarily in layer II‐III. However, approximately 10‐20% of the callosal projection and 20–40% of the projection to V‐II originated in layers IV and V. In contrast, the projection to the dorsal lateral geniculate nucleus originated nearly exclusively in layer VI, while corticotectal neurons occurred primarily in layer V. A significant number of corticotectal neurons were, however, found in layer IV. Thus, the above efferent systems were found to differ in their principal laminar origin and in the diffuseness of that origin. The origins of corticocortical projections were considerably more diffuse than those of corticofugal projections.

[1]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[2]  W. Singer,et al.  Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. , 1975, Journal of neurophysiology.

[3]  H. S. Gasser UNMEDULLATED FIBERS ORIGINATING IN DORSAL ROOT GANGLIA , 1950, The Journal of general physiology.

[4]  J. Schlag,et al.  Determination of antidromic excitation by the collision test: Problems of interpretation , 1976, Brain Research.

[5]  J. Hedreen,et al.  Observations on labeling of neuronal cell bodies, axons, and terminals after injection of horseradish peroxidase into rat brain , 1977, The Journal of comparative neurology.

[6]  W. C. Hall,et al.  Connections of layer VI in striate cortex of the grey squirrel (Sciurus carolinensis) , 1975, Brain Research.

[7]  H. H. Magalha˜es-Castro,et al.  Identification of corticotectal cells of the visual cortex of cats by means of horseradish peroxidase , 1975, Brain Research.

[8]  M. Wong-Riley Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys , 1979, Brain Research.

[9]  K. Chow,et al.  Anatomical studies of a temporal visual area in the rabbit , 1977, The Journal of comparative neurology.

[10]  J. Halperin,et al.  A study of the dynamics of retrograde transport and accumulation of horseradish peroxidase in injured neurons , 1975, Brain Research.

[11]  H. Nauta,et al.  Afferents to the rat caudoputamen studied with horseradish peroxidase. An evaluation of a retrograde neuroanatomical research method. , 1974, Brain research.

[12]  G. Raisman,et al.  A comparison of anterograde and retrograde axonal transport of horseradish peroxidase in the connections of the mammillary nuclei in the rat , 1975, Brain Research.

[13]  H. Swadlow,et al.  Interhemispheric striate projections in the prosimian primate, Galago senegalensis. , 1980, Brain, behavior and evolution.

[14]  S G Waxman,et al.  Regional differentiation of the axon: a review with special reference to the concept of the multiplex neuron. , 1972, Brain research.

[15]  H. Swadlow Properties of antidromically activated callosal neurons and neurons responsive to callosal input in rabbit binocular cortex. , 1974, Experimental neurology.

[16]  I. Parnas,et al.  Differential flow of information into branches of a single axon. , 1973, Brain research.

[17]  G. Innocenti,et al.  Morphological correlates of visual field transformation in the corpus callosum , 1976, Neuroscience Letters.

[18]  W Rall,et al.  Changes of action potential shape and velocity for changing core conductor geometry. , 1974, Biophysical journal.

[19]  H. Swadlow,et al.  Variations in conduction velocity and excitability following single and multiple impulses of visual callosal axons in the rabbit , 1976, Experimental Neurology.

[20]  E. G. Jones,et al.  Possible determinants of the degree of retrograde neuronal labeling with horseradish peroxidase , 1975, Brain Research.

[21]  C. Shatz Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats , 1977, The Journal of comparative neurology.

[22]  H. Kuypers,et al.  Single mammillary body cells with divergent axon collaterals. Demonstration by a simple, fluorescent retrograde double labeling technique in the rat , 1978, Brain Research.

[23]  J. Lund,et al.  Monkey retinal ganglion cells: Morphometric analysis and tracing of axonal projections, with a consideration of the peroxidase technique , 1975, The Journal of comparative neurology.

[24]  R. B. Freeman,et al.  Line length selective masking , 1976, Brain Research.

[25]  R. Rhoades,et al.  Visual callosal connections in the golden hamster , 1980, Brain Research.

[26]  K. Albus,et al.  Spiny stellates as cells of origin of association fibres from area 17 to area 18 in the cat's neocortex , 1981, Brain Research.

[27]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[28]  Theodore G. Weyand,et al.  The cells of origin of the corpus callosum in rabbit visual cortex , 1978, Brain Research.

[29]  R. Giolli,et al.  An autoradiographic study of the projection of visual cortical area 1 to the thalamus, pretectum and superior colliculus of the rabbit , 1978, The Journal of comparative neurology.

[30]  J. Hursh CONDUCTION VELOCITY AND DIAMETER OF NERVE FIBERS , 1939 .

[31]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

[32]  M. Wong-Riley Endogenous peroxidatic activity in brain stem neurons as demonstrated by their staining with diaminobenzidine in normal squirrel monkeys , 1976, Brain Research.

[33]  Y Hayashi,et al.  Recurrent collateral inhibition of visual cortical cells projecting to superior colliculus in cats. , 1969, Vision research.

[34]  B L Finlay,et al.  Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. , 1976, Journal of neurophysiology.

[35]  H. Swadlow Relationship of the corpus callosum to visual areas I and II of the awake rabbit , 1977, Experimental Neurology.

[36]  J. H. Casseday,et al.  Projections from cortex to tectum in the tree shrew, Tupaia glis , 1979, The Journal of comparative neurology.

[37]  D. Raczkowski,et al.  Connections of the striate cortex inGalago senegalensis , 1978, Brain Research.

[38]  L. Chalupa,et al.  Functional and anatomical consequences of neonatal visual cortical damage in superior colliculus of the golden hamster. , 1978, Journal of neurophysiology.

[39]  S L BeMent,et al.  A model for electrical stimulation of central myelinated fibers with monopolar electrodes. , 1969, Experimental neurology.

[40]  L. Palmer,et al.  Visual receptive fields of single striate corical units projecting to the superior colliculus in the cat. , 1974, Brain research.

[41]  C. Blakemore,et al.  Projections to the visual cortex in the golden hamster , 1979, The Journal of comparative neurology.

[42]  J. Stone,et al.  Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. , 1976, Journal of neurophysiology.

[43]  M. Mesulam,et al.  The blue reaction product in horseradish peroxidase neurohistochemistry: incubation parameters and visibility. , 1976, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[44]  A. Harvey A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat. , 1980, The Journal of physiology.

[45]  P. Molton,et al.  Survival of Common Terrestrial Microorganisms under Simulated Jovian Conditions , 1972, Nature.

[46]  W. Rushton A theory of the effects of fibre size in medullated nerve , 1951, The Journal of physiology.

[47]  W. B. Spatz,et al.  Golgi-like staining of neocortical neurons using retrogradely transported horseradish peroxidase , 1976, Neuroscience Letters.

[48]  J. Eccles,et al.  Intracellular recording from antidromically activated motoneurones , 1953, The Journal of physiology.

[49]  T. Tsumoto,et al.  Three groups of cortico‐geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex , 1980, The Journal of comparative neurology.

[50]  H. Swadlow,et al.  Modulation of impulse conduction along the axonal tree. , 1980, Annual review of biophysics and bioengineering.

[51]  R. Marrocco,et al.  Sustained and transient cells in monkey lateral geniculate nucleus: conduction velocites and response properties. , 1976, Journal of neurophysiology.

[52]  M. Bennett,et al.  Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. , 1972, Nature: New biology.

[53]  R. Giolli,et al.  Corticocortical fiber connections of the rabbit visual cortex: A fiber degeneration study , 1977, The Journal of comparative neurology.

[54]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[55]  L. Heimer,et al.  The afferent connections of the main and the accessory olfactory bulb formations in the rat: An experimental HRP‐study , 1978, The Journal of comparative neurology.

[56]  S. A. Talbot,et al.  Visual areas I and II of cerebral cortex of rabbit. , 1950, Federation proceedings.

[57]  B. P. Choudhury,et al.  VISUAL FIELD PROJECTION ON THE DORSAL NUCLEUS OF THE LATERAL GENICULATE BODY IN THE RABBIT. , 1965, Quarterly Journal of Experimental Physiology and Cognate Medical Sciences.

[58]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[59]  W. Burke,et al.  Single‐unit recording from antidromically activated optic radiation neurones , 1962, The Journal of physiology.

[60]  P. Schiller,et al.  Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. , 1978, Journal of neurophysiology.

[61]  Stephen G. Waxman,et al.  Ultrastructure of visual callosal axons in the rabbit , 1976, Experimental Neurology.

[62]  A L Pearlman,et al.  Laminar distribution of receptive field properties in the primary visual cortex of the mouse , 1980, The Journal of comparative neurology.