Passive cable properties and morphological correlates of neurones in the lateral geniculate nucleus of the cat.

1. We used an in vivo preparation of the cat to study the passive cable properties of sixteen X and twelve Y cells in the lateral geniculate nucleus. Cells were modelled as equivalent cylinders according to Rall's formulations (Rall, 1959a, 1969, 1977). We injected intracellular current pulses into these geniculate neurones, and we analysed the resulting voltage transients to obtain the cable parameters of these cells. In addition, fifty‐four physiologically characterized neurones were labelled with horseradish peroxidase (HRP) and analysed morphologically. 2. Analysis of HRP‐labelled geniculate neurones showed that the dendritic branching pattern of these cells adheres closely to the 3/2 power rule. That is, at each branch point, the diameter of the parent branch raised to the 3/2 power equals the sum of the diameters of the daughter dendrites after each is raised to the 3/2 power. Furthermore, preliminary data indicate that the dendritic terminations emanating from each primary dendrite occur at the same electrotonic distance from the soma. These observations suggest that both X and Y cells meet the geometric constraints necessary for reduction of their dendritic arbors into equivalent cylinders. 3. We found a strong linear relationship between the diameter of each primary dendrite and the membrane surface area of the arbor emanating from it. We used this relationship to derive an algorithm for determining the total somatic and dendritic membrane surface area of an X and Y cell simply from knowledge of the diameters of its soma and primary dendrites. 4. Both geniculate X and Y cells display current‐voltage relationships that were linear within +/‐ 20 mV of the resting membrane potential. This meant that we could easily remain within the linear voltage range during the voltage transient analyses. 5. X and Y cells clearly differ in terms of many of their electrical properties, including input resistance, membrane time constant and electrotonic length. The difference in input resistance between X and Y cells cannot be attributed solely to the smaller average size of X cells, but it also reflects a higher specific membrane resistance (Rm) of the X cells. Furthermore, X cells exhibit electrotonic lengths slightly larger than those of Y cells, but both neuronal types display electrotonic lengths of roughly 1. This indicates that even the most distally located innervation to these cells should have considerable influence on their somatic and axonal responses.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  W. Crill,et al.  Specific membrane properties of cat motoneurones , 1974, The Journal of physiology.

[2]  M Sur,et al.  Retinogeniculate terminations in cats: morphological differences between X and Y cell axons. , 1982, Science.

[3]  K. Sanderson,et al.  The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat , 1971, The Journal of comparative neurology.

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

[5]  R. Burke,et al.  Electrotonic characteristics of alpha motoneurones of varying size , 1971, The Journal of physiology.

[6]  R Iansek,et al.  An analysis of the cable properties of spinal motoneurones using a brief intracellular current pulse , 1973, The Journal of physiology.

[7]  J. Adams,et al.  Technical considerations on the use of horseradish peroxidase as a neuronal marker , 1977, Neuroscience.

[8]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[9]  S. Cullheim,et al.  A quantitative light microscopic study of the dendrites of cat spinal γ‐motoneurons after intracellular staining with horseradish peroxidase , 1981, The Journal of comparative neurology.

[10]  B. Gustafsson,et al.  Relations among passive electrical properties of lumbar alpha‐motoneurones of the cat. , 1984, The Journal of physiology.

[11]  W. Levy,et al.  Dendritic caliber and the 3/2 power relationship of dentate granule cells , 1984, The Journal of comparative neurology.

[12]  Michael J. O'Donovan,et al.  An HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons , 1982, The Journal of Comparative Neurology.

[13]  M Steriade,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: mechanisms of long-lasting hyperpolarizations. , 1984, Journal of neurophysiology.

[14]  J. Kellerth,et al.  Electrophysiological and morphological measurements in cat gastrocnemius and soleus α-motoneurones , 1984, Brain Research.

[15]  D. Hubel,et al.  Integrative action in the cat's lateral geniculate body , 1961, The Journal of physiology.

[16]  T. Poggio,et al.  A theoretical analysis of electrical properties of spines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[18]  G. Ahlsén,et al.  Inhibition from the brain stem of inhibitory interneurones of the cat's dorsal lateral geniculate nucleus. , 1984, The Journal of physiology.

[19]  J. Stone,et al.  Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. , 1972, Journal of neurophysiology.

[20]  J. Jack,et al.  An electrical description of the motoneurone, and its application to the analysis of synaptic potentials , 1971, The Journal of physiology.

[21]  T. Poggio,et al.  Retinal ganglion cells: a functional interpretation of dendritic morphology. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  S. Sherman Functional organization of the W-, X-, and Y- cell pathways in the cat: A review and hypothesis , 1985 .

[23]  W. Rall Time constants and electrotonic length of membrane cylinders and neurons. , 1969, Biophysical journal.

[24]  M. Ito,et al.  Electrical behaviour of the motoneurone membrane during intracellularly applied current steps. , 1965, The Journal of physiology.

[25]  János Szentágothai,et al.  Neuronal and Synaptic Architecture of the Lateral Geniculate Nucleus , 1973 .

[26]  T. A. Harrison,et al.  Differential effect of midbrain stimulation on X-sustained and Y-transient neurons in the lateral geniculate nucleus of the cat , 1977, Brain Research.

[27]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

[28]  A. G. Brown,et al.  Direct observations on the contacts made between Ia afferent fibres and alpha‐motoneurones in the cat's lumbosacral spinal cord. , 1981, The Journal of physiology.

[29]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[30]  S. Sherman,et al.  Morphological and physiological properties of geniculate W-cells of the cat: a comparison with X- and Y-cells. , 1983, Journal of neurophysiology.

[31]  M. Deschenes,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. , 1984, Journal of neurophysiology.

[32]  R. Shapley,et al.  Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. , 1981, Journal of neurophysiology.

[33]  Jonathan Stone,et al.  Hierarchical and parallel mechanisms in the organization of visual cortex , 1979, Brain Research Reviews.

[34]  A. L. Humphrey,et al.  Projection patterns of individual X‐ and Y‐cell axons from the lateral geniculate nucleus to cortical area 17 in the cat , 1985, The Journal of comparative neurology.

[35]  Joachim Krauth,et al.  The interpretation of significance tests for independent and dependent samples , 1983, Journal of Neuroscience Methods.

[36]  P. Nelson,et al.  Some electrical measurements of motoneuron parameters. , 1970, Biophysical journal.

[37]  Daniel J. Uhlrich,et al.  Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat , 1985, Nature.

[38]  R Fernald,et al.  An improved method for plotting retinal landmarks and focusing the eyes. , 1971, Vision research.

[39]  R Porter,et al.  The time course of minimal excitory post-synaptic potentials evoked in spinal motoneurones by group Ia afferent fibres. , 1971, The Journal of physiology.

[40]  W. Rall Branching dendritic trees and motoneuron membrane resistivity. , 1959, Experimental neurology.

[41]  S. Sherman,et al.  Synaptic circuits involving an individual retinogeniculate axon in the cat , 1987, The Journal of comparative neurology.

[42]  M. Egger,et al.  Quantitative morphological analysis of spinal motoneurons , 1982, Brain Research.

[43]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[44]  D. Durand,et al.  Electrotonic parameters of rat dentate granule cells measured using short current pulses and HRP staining. , 1983, Journal of neurophysiology.

[45]  E Kaplan,et al.  Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. , 1979, The Journal of physiology.

[46]  S. Bloomfield,et al.  Electroanatomy of a unique amacrine cell in the rabbit retina. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[47]  W Singer,et al.  Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. , 1977, Physiological reviews.

[48]  T. H. Brown,et al.  Electrotonic structure and specific membrane properties of mouse dorsal root ganglion neurons. , 1981, Journal of neurophysiology.

[49]  C. Nicholson Electric current flow in excitable cells J. J. B. Jack, D. Noble &R. W. Tsien Clarendon Press, Oxford (1975). 502 pp., £18.00 , 1976, Neuroscience.

[50]  S. Ellias,et al.  The dendritic varicosity: a mechanism for electrically isolating the dendrites of cat retinal amacrine cells? , 1980, Brain Research.

[51]  S. Sherman,et al.  Organization of visual pathways in normal and visually deprived cats. , 1982, Physiological reviews.

[52]  J. Capowski,et al.  Morphology of HRP-injected spinocervical tract neurons: effect of dorsal rhizotomy , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  P. Lennie,et al.  Spatial frequency analysis in the visual system. , 1985, Annual review of neuroscience.

[54]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

[55]  D A Turner,et al.  Steady-state electrotonic analysis of intracellularly stained hippocampal neurons. , 1980, Journal of neurophysiology.

[56]  S. Sherman,et al.  Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[57]  W. Singer,et al.  The effect of mesencephalic reticular stimulation on intracellular potentials of cat lateral geniculate neurons. , 1973, Brain research.

[58]  T. H. Brown,et al.  Passive electrical constants in three classes of hippocampal neurons. , 1981, Journal of neurophysiology.

[59]  C. Koch,et al.  Electrical properties of dendritic spines , 1983, Trends in Neurosciences.

[60]  A. Hodgkin,et al.  The electrical constants of a crustacean nerve fibre , 1946, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[61]  R. W. Guillery,et al.  A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat , 1969 .

[62]  Y. Ben-Ari,et al.  Inhibitory conductance changes and action of γ-aminobutyrate in rat hippocampus , 1981, Neuroscience.