Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex

Postnatal development of the primate cerebral cortex involves an initial proliferation and the subsequent attrition of cortical synapses. Although these maturational changes in synaptic density have been observed across the cortical mantle, little is known about the precise time course of developmental refinements in synaptic inputs to specific populations of cortical neurons. We examined the postnatal development of two markers of excitatory and inhibitory inputs to a subpopulation of layer III pyramidal neurons in area 9 and 46 of rhesus monkey prefrontal cortex. These neurons are of particular interest because they play a major role in the flow of information both within and between cortical regions. Quantitative reconstructions of Golgi-impregnated mid-layer III pyramidal neurons revealed substantial developmental changes in the relative density of dendritic spines, the major site of excitatory inputs to these neurons. Relative spine density on both the apical and basilar dendritic trees increased by 50% during the first two postnatal months, remained at a plateau through 1.5 years of age, and then decreased over the peripubertal age range until stable adult levels were achieved. As a measure of the postnatal changes in inhibitory input to the axon initial segment of these pyramidal neurons, we determined the density of parvalbumin-immunoreactive axon terminals belonging to the chandelier class of local circuit neurons. The density of these distinctive axon terminals (cartridges) exhibited a temporal pattern of change that exactly paralleled the changes in dendritic spine density. These results suggest that subpopulations of cortical neurons may be regulated by dynamic interactions between excitatory and inhibitory inputs during development and, in concert with other data, they emphasize the cellular specificity of postnatal refinements in cortical circuitry.

[1]  I Fariñas,et al.  Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. I. The cell body , 1991, The Journal of comparative neurology.

[2]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[3]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[4]  M. Arbib,et al.  Conceptual models of neural organization. , 1974, Neurosciences Research Program bulletin.

[5]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. III. Origins and frequency of occurrence of the terminals , 1992, Journal of neurocytology.

[6]  J. B. Levitt,et al.  Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46) , 1993, The Journal of comparative neurology.

[7]  M. Colonnier.  Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[8]  A. Peters,et al.  Chandelier cells in rat visual cortex , 1982, The Journal of comparative neurology.

[9]  J. Lund,et al.  Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics , 1993, The Journal of comparative neurology.

[10]  Françoise Condé,et al.  Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology , 1994, The Journal of comparative neurology.

[11]  J. Lund,et al.  Spine formation and maturation of type 1 synapses on spiny stellate neurons in primate visual cortex , 1983, The Journal of comparative neurology.

[12]  A. Peters,et al.  The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): A golgi‐electron microscopic study , 1985, The Journal of comparative neurology.

[13]  E G Jones,et al.  Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Goldman-Rakic,et al.  Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[15]  I. Feinberg,et al.  Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? , 1982, Journal of psychiatric research.

[16]  D. Rosenberg,et al.  Postnatal maturation of the dopaminergic innervation of monkey prefrontal and motor cortices: A tyrosine hydroxylase immunohistochemical analysis , 1995, The Journal of comparative neurology.

[17]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

[18]  M. Akil,et al.  Differential distribution of parvalbumin-immunoreactive pericellular clusters of terminal boutons in developing and adult monkey neocortex , 1992, Experimental Neurology.

[19]  R. S. Sloviter.  Calcium‐binding protein (calbindin‐D28k) and parvalbumin immunocytochemistry: Localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity , 1989, The Journal of comparative neurology.

[20]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[21]  M Marin-Padilla,et al.  The chandelier cell of the human visual cortex: A Golgi study , 1987, The Journal of comparative neurology.

[22]  D. Lewis,et al.  Postnatal development of the cholecystokinin innervation of monkey prefrontal cortex , 1993, The Journal of comparative neurology.

[23]  P. Somogyi,et al.  Glutamate decarboxylase‐immunoreactive terminals of Golgi‐impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex , 1983, The Journal of comparative neurology.

[24]  I Fariñas,et al.  Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The axon initial segment , 1991, The Journal of comparative neurology.

[25]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes , 1993, The Journal of comparative neurology.

[26]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[27]  P. Huttenlocher.  Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[28]  S. Sesack,et al.  Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA‐immunoreactive dendrites in rat and monkey cortex , 1995, The Journal of comparative neurology.

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

[30]  C. Horner,et al.  Methods of estimation of spine density--are spines evenly distributed throughout the dendritic field? , 1991, Journal of anatomy.

[31]  J. Nagy,et al.  Analysis of parvalbumin and calbindin D28k-immunoreactive neurons in dorsal root ganglia of rat in relation to their cytochrome oxidase and carbonic anhydrase content , 1989, Neuroscience.

[32]  J. Wolff,et al.  Synaptic reorganization in developing and adult nervous systems. , 1992, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[33]  P. Goldman-Rakic,et al.  Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. , 1993, Cerebral cortex.

[34]  M. Gayoso,et al.  A versatile and simple method for staining nervous tissue using Giemsa dye , 1985, Journal of Neuroscience Methods.

[35]  J. Lund,et al.  Postnatal development of thalamic recipient neurons in the monkey striate cortex: Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons , 1991, The Journal of comparative neurology.

[36]  D. Weinberger.  Implications of normal brain development for the pathogenesis of schizophrenia. , 1987, Archives of general psychiatry.

[37]  J. Lund,et al.  Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin‐releasing factor‐and parvalbumin‐immunoreactive populations , 1990, The Journal of comparative neurology.

[38]  P. Huttenlocher,et al.  The development of synapses in striate cortex of man. , 1987, Human neurobiology.

[39]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[40]  P. Goldman-Rakic,et al.  The synaptology of parvalbumin‐immunoreactive neurons in the primate prefrontal cortex , 1992, The Journal of comparative neurology.

[41]  A. Cowey,et al.  The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey , 1982, Neuroscience.

[42]  F. Valverde,et al.  A specialized type of neuron in the visual cortex of cat: A Golgi and electron microscope study of chandelier cells , 1980, The Journal of comparative neurology.

[43]  T. Powell,et al.  A combined golgi-electron microscopic study of the synapses made by the proximal axon and recurrent collaterals of a pyramidal cell in the somatic sensory cortex of the monkey , 1981, Neuroscience.

[44]  Differential laminar distribution of tyrosine hydroxylase-immunoreactive axons in infant and adult monkey prefrontal cortex , 1991, Neuroscience Letters.

[45]  P S Goldman-Rakic,et al.  Light and electron microscopic characterization of dopamine‐immunoreactive axons in human cerebral cortex , 1992, The Journal of comparative neurology.

[46]  J. E. Vaughn,et al.  Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex , 1983, Journal of neurocytology.

[47]  J. Lund.  Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[48]  P. Rakić,et al.  Synaptogenesis in monkey somatosensory cortex. , 1991, Cerebral cortex.

[49]  D. Schmechel,et al.  Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory‐motor cortex , 1985, The Journal of comparative neurology.

[50]  P S Goldman-Rakic,et al.  Synchronized overproduction of neurotransmitter receptors in diverse regions of the primate cerebral cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[51]  J. Lund,et al.  Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the Macaque monkey , 1975 .

[52]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[53]  S. Hsu,et al.  Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[54]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.

[56]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[57]  T. Powell,et al.  A study of the axon initial segment and proximal axon of neurons in the primate motor and somatic sensory cortices. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[58]  P. Rakić,et al.  Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. , 1989, Brain research. Developmental brain research.

[59]  P S Goldman-Rakic,et al.  Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. , 1982, Brain research.

[60]  P S Goldman-Rakic,et al.  Synaptogenesis in the prefrontal cortex of rhesus monkeys. , 1994, Cerebral cortex.

[61]  T. Kemper,et al.  The neuronographic and metric study of the dendritic arbours of neurons in the motor cortex of Macaca mulatta at birth and at 24 months of age. , 1973, Brain : a journal of neurology.