Laminar specificity of functional input to distinct types of inhibitory cortical neurons

Journal of Neuroscience

Volumn 29, Issue 1, 2009, Pages 70-85

  Xu, Xiangmin ^a,b   Callaway, Edward M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Barrel cortex; GFP; Interneurons; Photostimulation; Somatosensory cortex; Transgenic

Indexed keywords

GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEIN;

ANIMAL TISSUE; ARTICLE; BASKET CELL; BIPOLAR INHIBITORY NEURON; BRAIN CELL; BURST SPIKING INHIBITORY NEURON; CELL TYPE; CHANDELIER CELL; CONTROLLED STUDY; EXCITATORY JUNCTION POTENTIAL; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY NERVE CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; IRREGULAR SPIKING INHIBITORY NEURON; MARTINOTTI CELL; MOUSE; NEUROGLIAFORM CELL; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REGULAR SPIKING INHIBITORY NEURON; SOMATOSENSORY CORTEX;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DENDRITES; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; MODELS, STATISTICAL; NERVE NET; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PROTEINS; SOMATOSENSORY CORTEX; SOMATOSTATIN; STATISTICS, NONPARAMETRIC;

EID: 58149379146     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4104-08.2009     Document Type: Article

References (37)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557-568.
2. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H (2003) A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38:805-817.
3. Borrell V, Yoshimura Y, Callaway EM (2005) Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation. J Neurosci Methods 143:151-158.
4. Briggs F, Callaway EM (2005) Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. Cereb Cortex 15:479-488.
5. Bureau I, von Saint Paul F, Svoboda K (2006) Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol 4:e382.
6. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611.
7. Cruikshank SJ, Lewis TJ, Connors BW (2007) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10:462-468.
8. Dantzker JL, Callaway EM (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701-707.
9. Galarreta M, Erdélyi F, Szabó G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 24:9770-9778.
10. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
11. Gonchar Y, Burkhalter A (1999) Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex. Cereb Cortex 9:683-696.
12. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
13. Halabisky B, Shen F, Huguenard JR, Prince DA (2006) Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96:834-845.
14. Holmgren C, Harkany T, Svennenfors B, Zilberter Y (2003) Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551:139-153.
15. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M (2007) Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10:743-753.
16. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
17. Kawaguchi Y, Kondo S (2002) Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
18. López-Bendito G, Sturgess K, Erdélyi F, Szabó G, Molnár Z, Paulsen O (2004) Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14:1122-1133.
19. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069-5082.
20. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
21. Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113-132.
22. Murphy GJ, Du Lac S (2001) Postnatal development of spike generation in rat medial vestibular nucleus neurons. J Neurophysiol 85:1899-1906.
23. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354-3368.
24. Schubert D, Kötter R, Zilles K, Luhmann HJ, Staiger JF (2003) Cell type-specific circuits of cortical layer IV spiny neurons. J Neurosci 23:2961-2970.
25. Shepherd GM, Svoboda K (2005) Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25:5670-5679.
26. Shepherd GM, Pologruto TA, Svoboda K (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277-289.
27. Shepherd GM, Stepanyants A, Bureau I, Chklovskii D, Svoboda K (2005) Geometric and functional organization of cortical circuits. Nat Neurosci 8:782-790.
28. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735-746.
29. Simon A, Oláh S, Molnár G, Szabadics J, Tamás G (2005) Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 25:6278-6285.
30. Somogyi P, Tamás G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26:113-135.
31. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C, Huang ZJ, Nelson SB (2006) Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9:99-107.
32. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13:25-32.
33. Tamás G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
34. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y (2008) Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315-330.
35. Xu X, Roby KD, Callaway EM (2006) Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499:144-160.
36. Yoshimura Y, Callaway EM (2005) Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 8:1552-1559.
37. Yoshimura Y, Dantzker JL, Callaway EM (2005) Excitatory cortical neurons form fine-scale functional networks. Nature 433:868-873.