Functions of very distal dendrites: experimental and computational studies of layer 1 synapses on neocortical pyramidal cells

Publisher Summary This chapter reviews an approach that combines quantitative morphology, physiology, and computational analysis to understandthe functions of a complex synaptic–neuronal interaction in the cortex. A variation of the in vitro slice of rat somatosensory neocortex examines the effectiveness of layer 1 inputs to pyramidal cells whose bodies lie 0.5–1 mm deeper, in layers 3 or 5. The horizontal fibers in layer 1 (HL1) were isolated by disconnecting all deeper horizontal fibers with a cut perpendicular to the surface, extending from just below layer 1 downward through subcortical white matter and Layer 1 was stimulated on one side of the cut and the response mediated by HL1 fibers passing to the other side was recorded extracellularly and intracellularly. Backward cortico–cortical projections, which end largely on distal apical dendrites in layer 1, are important for higher cortical functions. By isolating horizontal afferents to layer 1 in an in vitro neocortical slice, layer 1 synapses can strongly excite pyramidal cells as deep as layer 5b.

[1]  J. Hablitz,et al.  EPSPs in rat neocortical neurons in vitro. II. Involvement of N-methyl-D-aspartate receptors in the generation of EPSPs. , 1989, Journal of neurophysiology.

[2]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[3]  C. Wilson,et al.  Capacitance compensation and bridge balance adjustment in intracellular recording from dendritic neurons , 1989, Journal of Neuroscience Methods.

[4]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.

[5]  KM Harris,et al.  Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  C. Stevens,et al.  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus , 1989, Nature.

[7]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[8]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[9]  Y Yarom,et al.  Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. , 1990, Journal of neurophysiology.

[10]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[11]  M. Bear,et al.  An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry , 1985, The Journal of comparative neurology.

[12]  D. Prince,et al.  Intradendritic recordings from hippocampal neurons. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Rolls Functions of neuronal networks in the hippocampus and neocortex in memory , 1989 .

[14]  A. Peters,et al.  The forms of non‐pyramidal neurons in the visual cortex of the rat , 1978, The Journal of comparative neurology.

[15]  A. Peters,et al.  A three dimensional study of layer I of the rat parietal cortex , 1973, The Journal of comparative neurology.

[16]  J Arezzo,et al.  Topography and intracranial sources of somatosensory evoked potentials in the monkey. I. Early components. , 1979, Electroencephalography and clinical neurophysiology.

[17]  M. Herkenham,et al.  New Perspectives on the Organization and Evolution of Nonspecific Thalamocortical Projections , 1986 .

[18]  H. Pockberger,et al.  Electrophysiological and morphological properties of rat motor cortex neurons in vivo , 1991, Brain Research.

[19]  W. Singer,et al.  Cholinergic innervation of the cat striate cortex: A choline acetyltransferase immunocytochemical analysis , 1986, The Journal of comparative neurology.

[20]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[21]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[22]  William R. Holmes,et al.  Effects of uniform and non-uniform synaptic ‘activation-distributions’ on the cable properties of modeled cortical pyramidal neurons , 1989, Brain Research.

[23]  Alan Peters,et al.  A technique for estimating total spine numbers on golgi‐impregnated dendrites , 1979, The Journal of comparative neurology.

[24]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[25]  Robert S. Morison,et al.  THE PRODUCTION OF RHYTHMICALLY RECURRENT CORTICAL POTENTIALS AFTER LOCALIZED THALAMIC STIMULATION , 1941 .

[26]  F. Bremer Inhibitions intrathalamiques récurrentielles et physiologie du sommeil , 1970 .

[27]  D. Prince,et al.  Sodium channels in dendrites of rat cortical pyramidal neurons. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Idan Segev,et al.  Compartmental models of complex neurons , 1989 .

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

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

[31]  J. Miller,et al.  Synaptic amplification by active membrane in dendritic spines , 1985, Brain Research.

[32]  B. Vogt The Role of Layer I in Cortical Function , 1991 .

[33]  D. Prince,et al.  Electrophysiology of isolated hippocampal pyramidal dendrites , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  G M Shepherd,et al.  Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. , 1991, Journal of neurophysiology.

[35]  W. Rall Membrane potential transients and membrane time constant of motoneurons. , 1960, Experimental neurology.

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

[37]  D. Prince,et al.  Transient expression of polysynaptic NMDA receptor-mediated activity during neocortical development , 1990, Neuroscience Letters.

[38]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

[39]  B. Connors,et al.  Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor‐mediated responses in neocortex of rat and cat. , 1988, The Journal of physiology.

[40]  R. Nicoll,et al.  The current excitement in long term potentiation , 1988, Neuron.

[41]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[42]  J. A. Foster,et al.  Intracortical origin of recruiting responses in the cat cortex. , 1980, Electroencephalography and clinical neurophysiology.

[43]  P. Andersen,et al.  A comparison of distal and proximal dendritic synapses on CA1 pyramids in guinea‐pig hippocampal slices in vitro , 1980, The Journal of physiology.

[44]  D. Shelton,et al.  Membrane resistivity estimated for the purkinje neuron by means of a passive computer model , 1985, Neuroscience.

[45]  O. Lindvall,et al.  Distribution of putative neurotransmitters in the neocortex , 1979, Neuroscience.

[46]  W. Levy,et al.  Insights into associative long-term potentiation from computational models of NMDA receptor-mediated calcium influx and intracellular calcium concentration changes. , 1990, Journal of neurophysiology.

[47]  M. Mignard,et al.  Paths of information flow through visual cortex. , 1991, Science.

[48]  T. H. Brown,et al.  Biophysical model of a Hebbian synapse. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. Schiller,et al.  Effect of cooling area 18 on striate cortex cells in the squirrel monkey. , 1982, Journal of neurophysiology.

[50]  I Segev,et al.  Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. , 1988, Journal of neurophysiology.

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