Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex

Nature Neuroscience

Volumn 10, Issue 4, 2007, Pages 462-468

  Cruikshank, Scott J ^a   Lewis, Timothy J ^b   Connors, Barry W ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ARTICLE; INTERNEURON; MOLECULAR DYNAMICS; MONOSYNAPTIC REFLEX; NEOCORTEX; NERVE CELL; NEUROTRANSMISSION; POSITIVE FEEDBACK; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; SYNAPSE; THALAMOCORTICAL TRACT; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; NEOCORTEX; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; SYNAPSES; THALAMUS;

EID: 33947647447     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1861     Document Type: Article

References (41)

1. Mountcastle, V.M. Perceptual Neuroscience (Harvard University Press, Cambridge, Massachusetts, USA, 1998).
2. Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79 (1999).
3. Porter, J.T., Johnson, C.K. & Agmon, A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci. 21, 2699-2710 (2001).
4. Bruno, R.M. & Simons, D.J. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J. Neurosci. 22, 10966-10975 (2002).
5. Swadlow, H.A. Thalamocortical control of feedforward inhibition in awake somatosensory 'barrel' cortex. Phil. Trans. R. Soc. Lond. B 357, 1717-1727 (2002).
6. Agmon, A. & Connors, B.W. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J. Neurosci. 12, 319-329 (1992).
7. Gil, Z. & Amitai, Y. Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J. Neurosci. 16, 6567-6578 (1996).
8. Beierlein, M., Gibson, J.R. & Connors, B.W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987-3000 (2003).
9. Gabernet, L., Jadhav, S.P., Feldman, D.E., Carandini, M. & Scanziani, M. Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48, 315-327 (2005).
10. Inoue, T. & Imoto, K. Feedforward inhibitory connections from multiple thalamic cells to multiple regular-spiking cells in layer 4 of the somatosensory cortex. J. Neurophysiol. 96, 1746-1754 (2006).
11. Sun, Q.Q., Huguenard, J.R. & Prince, D.A. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J. Neurosci. 26, 1219-1230 (2006).
12. Miller, K.D., Pinto, D.J. & Simons, D.J. Processing in layer 4 of the neocortical circuit: new insights fromvisual and somatosensory cortex. Curr. Opin. Neurobiol. 11, 488-497 (2001).
13. Douglas, R.J. & Martin, K.A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419-451 (2004).
14. Alonso, J.M. & Swadlow, H.A. Thalamocortical specificity and the synthesis of sensory cortical receptive fields. J. Neurophysiol. 94, 26-32 (2005).
15. Agmon, A. & Connors, B.W. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365-379 (1991).
16. Lawrence, J.J. & McBain, C.J. Interneuron diversity series: containing the detonation-feedforward inhibition in the CA3 hippocampus. Trends Neurosci. 26, 631-640 (2003).
17. Jonas, P., Bischofberger, J., Fricker, D. & Miles, R. Interneuron diversity series: fast in, fast out - temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci. 27, 30-40 (2004).
18. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446 (2003).
19. McNaughton, B.L., Barnes, C.A. & Andersen, P. Synaptic efficacy and EPSP summation in granule cells of rat fascia dentata studied in vitro. J. Neurophysiol. 46, 952-966 (1981).
20. Staiger, J.F., Zilles, K. & Freund, T.F. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur. J. Neurosci. 8, 2273-2285 (1996).
21. Martina, M., Royer, S. & Pare, D. Cell type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J. Neurophysiol. 86, 2887-2895 (2001).
22. Owens, D.F. & Kriegstein, A.R. Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727 (2002).
23. Gulledge, A.T. & Stuart, G.J. Excitatory actions of GABA in the cortex. Neuron 37, 299-309 (2003).
24. - extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J. Neurophysiol. 93, 2117-2126 (2005).
25. Szabadics, J. et al. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311, 233-235 (2006).
26. Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969-1985 (2001).
27. Bruno, R.M. & Sakmann, B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622-1627 (2006).
28. Higley, M.J. & Contreras, D. Balanced excitation and inhibition determine spike timing during frequency adaptation. J. Neurosci. 26, 448-457 (2006).
29. Galarreta, M. & Hestrin, S. Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292, 2295-2299 (2001).
30. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204 (1995).
31. Lambolez, B., Ropert, N., Perrais, D., Rossier, J. & Hestrin, S. Correlation between kinetics and RNA splicing of α-amino-3-hydroxy-5- methylisoxazole-4-propionic acid receptors in neocortical neurons. Proc. Natl. Acad. Sci. USA 93, 1797-1802 (1996).
32. Zhou, F.M. & Hablitz, J.J. AMPA receptor-mediated EPSCs in rat neocortical layer II/III interneurons have rapid kinetics. Brain Res. 780, 166-169 (1998).
33. Geiger, J.R., Lubke, J., Roth, A., Frotscher, M. & Jonas, P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023 (1997).
34. Walker, H.C., Lawrence, J.J. & McBain, C.J. Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents. Neuron 35, 161-171 (2002).
35. Benshalom, G. & White, E.L. Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J. Comp. Neurol. 253, 303-314 (1986).
36. Keller, A. & White, E.L. Synaptic organization of GABAergic neurons in the mouse SmI cortex. J. Comp. Neurol. 262, 1-12 (1987).
37. Ahmed, B., Anderson, J.C., Douglas, R.J., Martin, K.A. & Nelson, J.C. Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J. Comp. Neurol. 341, 39-49 (1994).
38. Ahmed, B., Anderson, J.C., Martin, K.A. & Nelson, J.C. Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J. Comp. Neurol. 380, 230-242 (1997).
39. Wilent, W.B. & Contreras, D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 8, 1364-1370 (2005).
40. Moore, C.I., Nelson, S.B. & Sur, M. Dynamics of neuronal processing in rat somatosensory cortex. Trends Neurosci. 22, 513-520 (1999).
41. Chattopadhyaya, B. et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611 (2004).