Cortical efferent control of subcortical sensory neurons by synaptic disinhibition

Cerebral Cortex

Volumn 17, Issue 9, 2007, Pages 2039-2049

  Henneberger, Christian ^a   Redman, Stephen J ^b   Grantyn, Rosemarie ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Biology and Environment   (Australia)

Author keywords

Developmental plasticity; Endocannabinoids; GABA release; mGluR; Visual cortex

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; ELECTROPHYSIOLOGY; EMBRYO; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSORY NERVE CELL; SUPERIOR COLLICULUS; SYNAPTIC INHIBITION; SYNAPTIC MEMBRANE; VISUAL CORTEX;

ANIMALS; CEREBRAL CORTEX; EFFERENT PATHWAYS; ELECTROPHYSIOLOGY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MICE; MICE, INBRED C57BL; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; PREGNANCY; SUPERIOR COLLICULUS; SYNAPSES; VISUAL CORTEX;

EID: 34548045545     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhl112     Document Type: Article

References (60)

1. Aamodt SM, Shi J, Colonnese MT, Veras W, Constantine-Paton M. 2000. Chronic NMDA exposure accelerates development of GABAergic inhibition in the superior colliculus. J Neurophysiol. 83:1580-1591.
2. Berardi N, Pizzorusso T, Maffei L. 2000. Critical periods during sensory development. Curr Opin Neurobiol. 10:138-145.
3. Bereshpolova Y, Stoelzel CR, Gusev AG, Bezdudnaya T, Swadlow HA. 2006. The impact of a corticotectal impulse on the awake superior colliculus. J Neurosci. 26:2250-2259.
4. Bernard C, Milh M, Morozov YM, Ben Ari Y, Freund TF, Gozlan H. 2005. Altering cannabinoid signaling during development disrupts neuronal activity. Proc Natl Acad Sci USA. 102:9388-9393.
5. Cardoso de Oliveira S, Hoffmann KP. 1995. The corticotectal projection of the rat in vitro: development, anatomy and physiological characteristics. Eur J Neurosci. 7:599-612.
6. Chen B, Schaevitz LR, McConnell SK. 2005. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci USA. 102:17184-17189.
7. Chevaleyre V, Castillo PE. 2003. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron. 38:461-472.
8. Chevaleyre V, Castillo PE. 2004. Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron. 43:871-881.
9. Cirone J, Sharp C, Jeffery G, Salt TE. 2002. Distribution of metabotropic glutamate receptors in the superior colliculus of the adult rat, ferret and cat. Neuroscience. 109:779-786.
10. Desai NS. 2003. Homeostatic plasticity in the CNS: synaptic and intrinsic forms. J Physiol (Paris). 97:391-402.
11. Diana MA, Bregestovski P. 2005. Calcium and endocannabinoids in the modulation of inhibitory synaptic transmission. Cell Calcium. 37:497-505.
12. Edwards DA, Kim J, Alger BE. 2006. Multiple mechanisms of endocannabinoid response initiation in hippocampus. J Neurophysiol. 95:67-75.
13. Freund TF, Katona I, Piomelli D. 2003. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev. 83:1017-1066.
14. Galante M, Diana MA. 2004. Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J Neurosci. 24:4865-4874.
15. Grantyn R, Jüttner R, Meier J. 2004. Development and use-dependent modification of synaptic connections in the visual layers of the rodent superior colliculus. In: Hall WC, Moschovakis A, editors. The superior colliculus. Boca Raton: CRC Press. p. 173-210.
16. Hashemi-Nezhad M, Wang C, Burke W, Dreher B. 2003. Area 21a of cat visual cortex strongly modulates neuronal activities in the superior colliculus. J Physiol. 550:535-552.
17. Hashimotodani Y, Ohno-Shosaku T, Tsubokawa H, Ogata H, Emoto K, Maejima T, Araishi K, Shin HS, Kano M. 2005. Phospholipase Cbeta serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron. 45:257-268.
18. Henneberger C, Jüttner R, Schmidt S, Walter JH, Meier J, Rothe T, Grantyn R. 2005. GluR- and TrkB-mediated maturation of GABA(A) receptor function during the period of eye opening. Eur J Neurosci. 21:431-440.
19. Henneberger C, Kirischuk S, Grantyn R. 2005. Brain-derived neurotrophic factor modulates GABAergic synaptic transmission by enhancing presynaptic glutamic acid decarboxylase 65 levels, promoting asynchronous release and reducing the number of activated postsynaptic receptors. Neuroscience. 135:749-763.
20. Hensch TK. 2005. Critical period plasticity in local cortical circuits. Nat Rev Neurosci. 6:877-888.
21. Huettner JE, Baughman RW. 1988. The pharmacology of synapses formed by identified corticocollicular neurons in primary cultures of rat visual cortex. J Neurosci. 8:160-175.
22. Inoue K, Terashima T, Inoue Y. 1992. Postnatal development of the corticotectal projection from the visual cortex of the mouse. Okajimas Folia Anat Jpn. 68:319-331.
23. Khachab MY, Bruce LL. 1999. The development of corticocollicular projections in anophthalmic mice. Brain Res Dev Brain Res. 114:179-192.
24. Kim J, Isokawa M, Ledent C, Alger BE. 2002. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci. 22:10182-10191.
25. Kirischuk S, Juettner R, Grantyn R. 2005. Time-matched pre- and postsynaptic changes of GABAergic synaptic transmission in the developing mouse superior colliculus. J Physiol. 563:795-807.
26. Kirmse K, Kirischuk S. 2006. Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci. 26:4216-4227.
27. Kreitzer AC, Regehr WG. 2001. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 29:717-727.
28. Leichnetz GR, Goldberg ME. 1988. Higher centers concerned with eye movements and visual attention: cerebral cortex and thalamus. In: Büttner-Ennever JA, editor. Neuroanatomy of the oculomotor system. Amsterdam: Elsevier. p. 365-429.
29. Lenz RA, Alger BE. 1999. Calcium dependence of depolarization-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. J Physiol. 521:147-157.
30. Llano I, Leresche N, Marty A. 1991. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron. 6:565-574.
31. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M. 2001. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron. 31:463-475.
32. Majdan M, Shatz CJ. 2006. Effects of visual experience on activitydependent gene regulation in cortex. Nat Neurosci. 9:650-659.
33. McIlwain JT. 1975. Visual receptive fields and their images in superior colliculus of the cat. J Neurophysiol. 38:219-230.
34. Meier J, Akyeli J, Kirischuk S, Grantyn R. 2003. GABA(A) receptor activity and PKC control inhibitory synaptogenesis in CNS tissue slices. Mol Cell Neurosci. 23:600-613.
35. Meier J, Jüttner R, Kirischuk S, Grantyn R. 2002. Synaptic anchoring of glycine receptors in developing collicular neurons under control of metabotropic glutamate receptor activity. Mol Cell Neurosci. 21:324-340.
36. Mize RR, Salt TE. 2004. Mechanisms underlying development of the retinocollicular pathway. In: Hall WC, Moschovakis A, editors. The superior colliculus. Boca Raton: CRC Press. p. 211-239.
37. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD. 2005. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron. 47:817-831.
38. Morishita W, Kirov SA, Alger BE. 1998. Evidence for metabotropic glutamate receptor activation in the induction of depolarization-induced suppression of inhibition in hippocampal CA1. J Neurosci. 18:4870-4882.
39. Novak N, Bolz J. 1993. Formation of specific efferent connections in organotypic slice cultures from rat visual cortex cocultured with lateral geniculate nucleus and superior colliculus. Eur J Neurosci. 5:15-24.
40. O'Leary DD, Bicknese AR, De Carlos JA, Heffner CD, Koester SE, Kutka LJ, Terashima T. 1990. Target selection by cortical axons: alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb Symp Quant Biol. 55:453-468.
41. O'Leary DD, Terashima T. 1988. Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and "waiting periods". Neuron. 1:901-910.
42. Ohno-Shosaku T, Hashimotodani Y, Maejima T, Kano M. 2005. Calcium signaling and synaptic modulation: regulation of endocannabinoid-mediated synaptic modulation by calcium. Cell Calcium. 38:369-374.
43. Perouansky M, Grantyn R. 1989. Separation of quisqualate- and kainate-selective glutamate-receptors in cultured neurons from the rat superior colliculus. J Neurosci. 9:70-80.
44. A responses in hippocampal pyramidal cells. J Neurosci. 12:4122-4132.
45. Rhoades RW, Figley B, Mooney RD, Fish SE. 1991. Development of the occipital corticotectal projection in the hamster. Exp Brain Res. 86:373-383.
46. Schoepp DD, Jane DE, Monn JA. 1999. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology. 38:1431-1476.
47. Shi J, Aamodt SM, Constantine-Paton M. 1997. Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J Neurosci. 17:6264-6276.
48. Singh B, Henneberger C, Betances D, Arevalo MA, Rodríguez- Tébar A, Meier JC, Grantyn R. 2006. Altered balance of glutamatergic/GABAergic synaptic input and associated changes in dendrite morphology after BDNF expression in BDNF-deficient hippocampal neurons. J Neurosci. 26:7189-7200.
49. Skaliora I, Doubell TP, Holmes NP, Nodal FR, King AJ. 2004. Functional topography of converging visual and auditory inputs to neurons in the rat superior colliculus. J Neurophysiol. 92:2933-2946.
50. Taschenberger H, Grantyn R. 1995. Synaptic current kinetics in a solely AMPA receptor-operated glutamatergic synapse formed by rat retinal ganglion neurons. J Neurophysiol. 74:1123-1136.
51. Thong IG, Dreher B. 1986. The development of the corticotectal pathway in the albino rat. Brain Res. 390:227-238.
52. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 83:393-411.
53. Tsou K, Nogueron MI, Muthian S, Sanudo-Pena MC, Hillard CJ, Deutsch DG, Walker JM. 1998. Fatty acid amide hydrolase is located preferentially in large neurons in the rat central nervous system as revealed by immunohistochemistry. Neurosci Lett. 254:137-140.
54. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY. 2002. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron. 34:289-300.
55. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci. 5:97-107.
56. Varma N, Carlson GC, Ledent C, Alger BE. 2001. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci. 21:RC188.
57. Weimann JM, Zhang YA, Levin ME, Devine WP, Brulet P, McConnell SK. 1999. Cortical neurons require Otx1 for the refinement of exuberant axonal projections to subcortical targets. Neuron. 24:819-831.
58. Wilson RI, Nicoll RA. 2001. Correction: endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 411:974.
59. Yamamoto N, Yamada K, Kurotani T, Toyama K. 1992. Laminar specificity of extrinsic cortical connections studied in coculture preparations. Neuron. 9:217-228.
60. Zheng W, Knudsen EI. 1999. Functional selection of adaptive auditory space map by GABAA-mediated inhibition. Science. 284:962-965.