Biocytin-labelling and its impact on late 20th century studies of cortical circuitry

Brain Research Reviews - Tập 66 - Trang 43-53 - 2011
Alex M. Thomson1, William E. Armstrong2
1Department of Pharmacology, The School of Pharmacy, University of London, 29-39, Brunswick Square, London WC1N 1AX UK
2Department of Anatomy and Neurobiology and Neuroscience Institute, University of Tennessee Health Science Center, 855 Monroe Avenue, Suite 515, Memphis, TN 38163, USA

Tài liệu tham khảo

Alexander, 2005, Presynaptic inhibition of corticothalamic feedback by metabotropic glutamate receptors, J. Neurophysiol., 94, 163, 10.1152/jn.01198.2004 Ali, 1998, Facilitating pyramid to horizontal O/A interneurone inputs : dual intracellular recordings in slices of rat hippocampus, J. Physiol., 507, 185, 10.1111/j.1469-7793.1998.185bu.x Ali, 2008, Synaptic α5 subunit containing GABAA receptors mediate IPSPs elicited by dendrite-targeting cells in rat neocortex, Cereb. Cortex, 18, 1260, 10.1093/cercor/bhm160 Ali, 1998, CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices, J. Physiol., 507, 201, 10.1111/j.1469-7793.1998.201bu.x Ali, 2007, Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in juvenile and adult neocortical slices, J. Physiol., 580.1, 149, 10.1113/jphysiol.2006.124214 Angulo, 1997, Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells, J. Neurosci, 17, 6685, 10.1523/JNEUROSCI.17-17-06685.1997 Armstrong, 1982, Spontaneous ‘phasic firing’ in supraoptic neurons recorded from hypothalamo-neurohypophysial explants in vitro, Neuroendocrinology, 34405 Armstrong, 1985, Evidence for excitatory actions of histamine on supraoptic neurons in vitro: mediation by an H1-type receptor, Neuroscience, 16, 307, 10.1016/0306-4522(85)90004-1 Armstrong, 1994, Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro, J. Physiol. (Lond)., 475, 115, 10.1113/jphysiol.1994.sp020053 Bannister, 2007, Dynamic properties of excitatory synaptic connections involving layer 4 pyramidal cells in adult rat and cat neocortex, Cereb. Cortex, 17, 2190, 10.1093/cercor/bhl126 Betz, 1970, Depression of transmitter release at the neuromuscular junction of the frog, J. Physiol., 206, 620, 10.1113/jphysiol.1970.sp009034 Binzegger, 2004, A quantitative map of the circuit of cat primary visual cortex, J. Neurosci., 24, 8441, 10.1523/JNEUROSCI.1400-04.2004 Branco, 2009, A multiplication and integration time window gradient in dendrites of cortical pyramidal neurons, Soc. Neurosci. Abstr, 315.6 Brémaud, 2007, Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex, PNAS, 104, 14134, 10.1073/pnas.0705661104 Brimble, 1977, Characterization of the responses of oxytocin- and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation, J. Physiol., 271, 253, 10.1113/jphysiol.1977.sp011999 Buhl, 1994, Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus, J. Neurophysiol., 71, 1289, 10.1152/jn.1994.71.4.1289 Buhl, 1996, Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro, Hippocampus, 6, 294, 10.1002/(SICI)1098-1063(1996)6:3<294::AID-HIPO7>3.0.CO;2-N Callaway, 2008, Transneuronal circuit tracing with neurotropic viruses, Curr. Opin. Neurobiol., 18, 617, 10.1016/j.conb.2009.03.007 Castro-Alamancos, 2002, Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs, J. Neurophysiol., 87, 946, 10.1152/jn.00426.2001 Chance, 1998, Synaptic depression and the temporal response characteristics of V1 cells, J. Neurosci., 18, 4785, 10.1523/JNEUROSCI.18-12-04785.1998 Cobb, 1995, Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons, Nature, 378, 75, 10.1038/378075a0 Connors, 1982, Electrophysiological properties of neocortical neurons in vitro, J. Neurophysiol., 48, 1302, 10.1152/jn.1982.48.6.1302 Cowan, 1994, Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex, J. Neurophysiol., 71, 17, 10.1152/jn.1994.71.1.17 Cullheim, 1976, Combined light and electron microscopic tracing of neurons, including axons and synaptic terminals, after intracellular injection of horseradish peroxidase, Neurosci. Lett., 2, 307, 10.1016/0304-3940(76)90165-8 Dale, 1934, Pharmacology and nerve-endings, Proc. Roy. Soc. Med., 28, 319, 10.1177/003591573502800330 DeFelipe, 2002, Cortical interneurons: from Cajal to 2001, Prog. Brain Res., 136, 215, 10.1016/S0079-6123(02)36019-9 Deuchars, 1995, Single axon fast IPSPs elicited by a sparsely spiny interneurone in rat neocortex, Neuroscience, 65, 935, 10.1016/0306-4522(95)00020-J Deuchars, 1995, Innervation of burst firing interneurones by pyramidal cells in deep layers of rat somatomotor cortex: paired intracellular recordings with biocytin filling, Neuroscience, 69, 739, 10.1016/0306-4522(95)00288-T Deuchars, 1996, CA1 pyramid–pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling, Neuroscience, 74, 1009 Deuchars, 1994, Relationships between morphology and physiology of pyramid–pyramid single axon connections in rat neocortex in vitro, J. Physiol., 478, 423, 10.1113/jphysiol.1994.sp020262 Dreifuss, 1976, Mammalian endocrine neurones: control of phasic activity by antidromic action potentials, Neurosci. Lett., 3, 281, 10.1016/0304-3940(76)90055-0 Erickson, 1990, Inward rectification (Ih) in immunocytochemically-identified vasopressin and oxytocin neurons of the guinea-pig supraoptic nucleus, J. Neuroendocrinol., 2, 261.s, 10.1111/j.1365-2826.1990.tb00402.x Fairén, 2007, Cajal and Lorente de Nó on cortical interneurons: coincidences and progress, Brain Res. Rev., 55, 430, 10.1016/j.brainresrev.2007.06.004 Feldmeyer, 2002, Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column, J. Physiol., 538, 803, 10.1113/jphysiol.2001.012959 Foehring, 1991, Correlation of physiologically and morphologically identified neuronal types in human association cortex in vitro, J. Neurophysiol., 66, 1825, 10.1152/jn.1991.66.6.1825 Fuentealba, 2008, Ivy Cells: A population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity, Neuron, 57, 917, 10.1016/j.neuron.2008.01.034 Geiger, 1995, Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS, Neuron, 15, 193, 10.1016/0896-6273(95)90076-4 Golgi, 1873, Sulla sostanza grigia del cervello, Gaz. Med. Ital. Lombardia, 6, 244 Granseth, 2002, Paired pulse facilitation of corticogeniculate EPSCs in the dorsal lateral geniculate nucleus of the rat investigated in vitro, J. Physiol., 544, 477, 10.1113/jphysiol.2002.024703 Han, 1993, A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus, Eur. J. NeuroSci., 5, 395, 10.1111/j.1460-9568.1993.tb00507.x Hatton, 1978, Spontaneous and osmotically stimulated activity in slices of rat hypothalamus, Brain Res. Bull., 3497 Hestrin, 1996, Morphology and physiology of cortical neurons in layer I, J. Neurosci., 16, 5290, 10.1523/JNEUROSCI.16-17-05290.1996 Horikawa, 1988, A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates, J Neurosci Meth., 25, 1, 10.1016/0165-0270(88)90114-8 Hughes, 2000, Double immuno-fluorescence, peroxidase labelling and ultrastructural analysis of interneurones following prolonged electrophysiological recordings in vitro, J. Neurosci. Meth., 101, 107, 10.1016/S0165-0270(00)00254-5 Jonas, 1994, Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression, Neuron, 12, 1281, 10.1016/0896-6273(94)90444-8 Jones, 2007, Neuroanatomy: Cajal and after Cajal, Brain Res. Rev., 55, 248, 10.1016/j.brainresrev.2007.06.001 Kang, 1990, Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata, Brain Res., 535, 79, 10.1016/0006-8993(90)91826-3 Katz, 1996, Neural transmitter release: from quantal secretion to exocytosis and beyond The Fenn Lecture, J. Neurocytol., 25, 677, 10.1007/BF02284834 Kawaguchi, 1992, Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents, J Neurophysiol., 67, 1669, 10.1152/jn.1992.67.6.1669 Kawaguchi, 1993, Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex, J Neurophysiol., 70, 387, 10.1152/jn.1993.70.1.387 Kawaguchi, 1996, Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex, J. Neurosci., 16, 2701, 10.1523/JNEUROSCI.16-08-02701.1996 Kawaguchi, 1997, GABAergic cell subtypes and their synaptic connections in rat frontal cortex, Cereb. Cortex, 7, 476, 10.1093/cercor/7.6.476 Kawaguchi, 1989, Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs, J. Neurophysiol., 62, 1052, 10.1152/jn.1989.62.5.1052 Kawaguchi, 1990, Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin, J. Neurosci., 10, 3421, 10.1523/JNEUROSCI.10-10-03421.1990 Kita, 1991, A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin, J. Neurosci. Methods, 37, 141, 10.1016/0165-0270(91)90124-I Kitai, 1976, Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase, Brain Res., 109, 601, 10.1016/0006-8993(76)90039-1 Klausberger, 2003, Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo, Nature, 421, 844, 10.1038/nature01374 Klausberger, 2004, Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo, Nat. Neurosci., 7, 41, 10.1038/nn1159 Klausberger, 2005, Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations, J. Neurosci., 25, 9782, 10.1523/JNEUROSCI.3269-05.2005 Knowles, 1981, Local circuit synaptic interactions in hippocampal brain slices, J. Neurosci., 1, 318, 10.1523/JNEUROSCI.01-03-00318.1981 Lacaille, 1987, Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology, J. Neurosci., 7, 1979, 10.1523/JNEUROSCI.07-07-01979.1987 Llinás, 1988, The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function, Science, 242, 1654, 10.1126/science.3059497 Llinás, 1982, Electrophysiology of mammalian thalamic neurones in vitro, Nature, 297, 406, 10.1038/297406a0 Llinás, 1988, Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation, J. Physiol., 404, 241, 10.1113/jphysiol.1988.sp017288 Llinás, 1980, Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices, J. Physiol., 305, 171, 10.1113/jphysiol.1980.sp013357 Markram, 1997, Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex, J. Physiol., 500, 409, 10.1113/jphysiol.1997.sp022031 Mercer, 2005, Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex, Cereb. Cortex, 15, 1485, 10.1093/cercor/bhi027 Möhler, 2002, A new benzodiazepine pharmacology, J. Pharmacol. Exp. Ther., 300, 2, 10.1124/jpet.300.1.2 Nyíri, 2003, Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus, Neuroscience, 119, 347, 10.1016/S0306-4522(03)00157-X Nusser, 1996, Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells, Proc. Natl. Acad. Sci. U. S. A., 93, 11939, 10.1073/pnas.93.21.11939 Nyíri, 2001, Input-dependent synaptic targeting of alpha(2)-subunit-containing GABAA receptors in synapses of hippocampal pyramidal cells of the rat, Eur. J. NeuroSci., 13, 428, 10.1046/j.1460-9568.2001.01407.x Pawelzik, 1999, Modulation of bistratified cell IPSPs and basket cell IPSPs by pentobarbitone sodium, diazepam and Zn2+: dual recordings in slices of adult rat hippocampus, Eur. J. Neurosci., 11, 3552, 10.1046/j.1460-9568.1999.00772.x Pawelzik, 2002, Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus, J. Comp. Neurol., 443, 346, 10.1002/cne.10118 Peters, 2007, Golgi, Cajal, and the fine structure of the nervous system, J. Brain Res. Rev., 55, 256, 10.1016/j.brainresrev.2006.12.002 Petreanu, 2009, The subcellular organization of neocortical excitatory connections, Nature, 457, 1142, 10.1038/nature07709 Porter, 1998, Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex, Eur. J. NeuroSci., 12, 3617, 10.1046/j.1460-9568.1998.00367.x Reyes, 1998, Target-cell-specific facilitation and depression in neocortical circuits, Nat. Neurosci., 1, 279, 10.1038/1092 Roper, 2003, AHP's, HAP's and DAP's: how potassium currents regulate the excitability of rat supraoptic neurones, J. Comput. Neurosci., 15, 367, 10.1023/A:1027424128972 Roper, 2004, Burst initiation and termination in phasic vasopressin cells of the rat supraoptic nucleus: a combined mathematical, electrical, and calcium fluorescence study, J. Neurosci., 24, 4818, 10.1523/JNEUROSCI.4203-03.2004 Scharfman, 1990, Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections, Neuroscience, 37, 693, 10.1016/0306-4522(90)90100-I Schwartzkroin, 1985, Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus, J. Comp. Neurol., 232, 205, 10.1002/cne.902320206 Schwartzkroin, 1978, Physiological and morphological identification of a nonpyramidal hippocampal cell type, Brain Res., 157, 1, 10.1016/0006-8993(78)90991-5 Shevchenko, 2004, High-threshold, Kv3-like potassium currents in magnocellular neurosecretory neurons and their role in spike repolarization, J. Neurophysiol., 92, 3043, 10.1152/jn.00431.2004 Smith, 1990, Tuberal supraoptic neurons—I Morphological and electrophysiological characteristics observed with intracellular recording and biocytin filling in vitro, Neuroscience, 38, 469, 10.1016/0306-4522(90)90043-4 Smith, 1993, Histamine enhances the depolarizing afterpotential of immunohistochemically identified vasopressin neurons in the rat supraoptic nucleus via H1-receptor activation, Neuroscience, 53, 855, 10.1016/0306-4522(93)90630-X Snow, 1976, Tracing axons and axon collaterals of spinal neurons using intracellular injection of horseradish peroxidase, Science, 191, 312, 10.1126/science.54936 Somogyi, 2005, Defined types of cortical interneurone structure space and spike timing in the hippocampus, J. Physiol., 562, 9, 10.1113/jphysiol.2004.078915 Somogyi, 1982, The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey, Neuroscience, 7, 2577, 10.1016/0306-4522(82)90086-0 Spruston, 2008, Pyramidal neurons: dendritic structure and synaptic integration, Nat. Rev. Neurosci., 9, 206, 10.1038/nrn2286 Stepanyants, 2008, Local potential connectivity in cat primary visual cortex, Cereb. Cortex, 18, 13, 10.1093/cercor/bhm027 Stern, 1995, Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro, J. Physiol. (Lond)., 488, 701, 10.1113/jphysiol.1995.sp021001 Stern, 1996, Changes in the electrical properties of supraoptic nucleus oxytocin and vasopressin neurons during lactation, J Neurosci., 16, 4861, 10.1523/JNEUROSCI.16-16-04861.1996 Stern, 1997, Sustained outward rectification of oxytocinergic neurones in the rat supraoptic nucleus: ionic dependence and pharmacology, J. Physiol. (Lond)., 500, 497, 10.1113/jphysiol.1997.sp022036 Stern, 1998, Reorganization of the dendritic trees of oxytocin and vasopressin neurons of the rat supraoptic nucleus during lactation, J Neurosci., 18, 841, 10.1523/JNEUROSCI.18-03-00841.1998 Stern, 1999, Differences in the properties of ionotropic glutamate synaptic currents in oxytocin and vasopressin neuroendocrine neurons, J. Neurosci., 19, 3367, 10.1523/JNEUROSCI.19-09-03367.1999 Stern, 2000, Enhanced neurotransmitter release at glutamatergic synapses on oxytocin neurones during lactation in the rat, J Physiol (Lond)., 526, 109, 10.1111/j.1469-7793.2000.t01-1-00109.x Stewart, 1981, Lucifer dyes—highly fluorescent dyes for biological tracing, Nature, 292, 17, 10.1038/292017a0 Storm, 1994, Evidence that excitability changes in presynaptic fibers may affect paired-pulse facilitation in hippocampal slices, Soc. Neurosci. Abstr., 20, 1339 Swanson, 2007, A century of neuroscience discovery: reflecting on the Nobel Prize to Golgi and Cajal in 1906, Brain Res. Rev., 55, 191, 10.1016/j.brainresrev.2007.07.001 Tamás, 2000, Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons, Nat. Neurosci., 3, 366, 10.1038/73936 Tarczy-Hornoch, 1999, Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro, Cereb. Cortex, 9, 833, 10.1093/cercor/9.8.833 Tasker, 1991, Comparison of three intracellular markers for combined electrophysiological, morphological and immunohistochemical analyses, J. Neurosci. Methods., 38, 129, 10.1016/0165-0270(91)90163-T Teruyama, 2002, Changes in the active membrane properties of rat supraoptic neurones during pregnancy and lactation, J. Neuroendocrinol., 14, 933, 10.1046/j.1365-2826.2002.00844.x Teruyama, 2005, Enhancement of calcium-dependent afterpotentials in oxytocin neurons of the rat supraoptic nucleus during lactation, J. Physiol., 566, 505, 10.1113/jphysiol.2005.085985 Teruyama, 2007, Calcium-dependent fast depolarizing afterpotentials in vasopressin neurons in the rat supraoptic nucleus, J. Neurophysiol., 98, 2612, 10.1152/jn.00599.2007 Teruyama, 2008, Central blockade of oxytocin receptors during mid-late gestation reduces the amplitude of slow afterhyperpolarization in the supraoptic oxytocin neurons, Am. J. Physiol. Endocrinol. Metab., 2951167 Thomson, 2003, Presynaptic frequency- and pattern-dependent filtering, J. Comput. Neurosci., 15, 159, 10.1023/A:1025812808362 Thomson AM (2010) Neocortical layer 6, a review (invited review — under review Frontiers). Thomson, 1998, Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex, Neuroscience, 84, 669, 10.1016/S0306-4522(97)00557-5 Thomson, 2003, Inter-laminar connections in the neocortex, Cereb. Cortex, 13, 5, 10.1093/cercor/13.1.5 Thomson AM, Jovanovic JN (2010) Mechanisms underlying synapse-specific clustering of GABAA receptors (invited review — under review EJN). Thomson, 2007, Functional maps of neocortical local circuitry, Front. Neurosci., 1, 19, 10.3389/neuro.01.1.1.002.2007 Thomson, 1993, Fluctuations in pyramid–pyramid EPSPs modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex, Neuroscience, 54, 329, 10.1016/0306-4522(93)90256-F Thomson, 2003, Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex, Cereb. Cortex, 13, 136, 10.1093/cercor/13.2.136 Thomson, 1993, Single axon EPSPs in neocortical interneurones exhibit pronounced paired pulse facilitation, Neuroscience, 54, 347, 10.1016/0306-4522(93)90257-G Thomson, 1993, Large, deep layer pyramid–pyramid, single axon EPSPs in slices of rat motor cortex display paired pulse and frequency dependent depression mediated presynaptically and self facilitation mediated postsynaptically, J. Neurophysiol., 70, 2354, 10.1152/jn.1993.70.6.2354 Thomson, 1995, Properties of single axon EPSPs elicited in spiny interneurones by action potentials in pyramidal neurones in slices of rat neocortex, Neuroscience, 69, 727, 10.1016/0306-4522(95)00287-S Thomson, 1996, Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex, J. Physiol., 496, 81, 10.1113/jphysiol.1996.sp021667 Thomson, 1996, Neocortical local synaptic circuitry revealed with dual intracellular recordings and biocytin-filling, J. Physiol. (Paris), 90, 211, 10.1016/S0928-4257(97)81425-8 Thomson, 1996, Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex, J. Physiol., 496, 81, 10.1113/jphysiol.1996.sp021667 Thomson, 2000, Differential sensitivity to Zolpidem of IPSPs activated by morphologically identified CA1 interneurones in slices of rat hippocampus, Eur. J. Neurosci., 12, 425, 10.1046/j.1460-9568.2000.00915.x Thomson, 2002, Target and temporal pattern selection at neocortical synapses, Phil Trans Roy Soc B., 357, 1781, 10.1098/rstb.2002.1163 Thomson, 2002, Synaptic connections and small circuits involving excitatory and inhibitory neurones in layers 2 to 5 of adult rat and cat neocortex: triple intracellular recordings and biocytin-labelling in vitro, Cereb. Cortex, 12, 936, 10.1093/cercor/12.9.936 Tsodyks, 1997, The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability, Proc. Natl Acad. Sci. USA, 94, 719, 10.1073/pnas.94.2.719 Tukker, 2007, Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo, J. Neurosci., 27, 8184, 10.1523/JNEUROSCI.1685-07.2007 West, 2006, Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs, Cereb. Cortex, 16, 200, 10.1093/cercor/bhi098 White, 2007, Reflections on the specificity of synaptic connections, Brain Res. Rev., 55, 422, 10.1016/j.brainresrev.2006.12.004 Wilson, 1990, Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum, J Neurosci., 10, 508, 10.1523/JNEUROSCI.10-02-00508.1990