Top-down dendritic input increases the gain of layer 5 pyramidal neurons

Cerebral Cortex

Volumn 14, Issue 10, 2004, Pages 1059-1070

  Larkum, Matthew E ^a   Senn, Walter ^a   Lüscher, Hans R ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

BAC firing; Calcium spike; Cortex; Dendrite; Gain; Pyramidal neuron

Indexed keywords

CALCIUM;

ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM CONDUCTANCE; CONTROLLED STUDY; DENDRITE; DEPOLARIZATION; ELECTRIC CURRENT; FREQUENCY MODULATION; INJECTION; NERVE CONDUCTION; NOISE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATIC CELL; SOMATOSENSORY CORTEX; SPIKE;

ACTION POTENTIALS; ANIMALS; DENDRITES; NEOCORTEX; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 4544222913     PISSN: 10473211     EISSN: None     Source Type: Journal    
DOI: 10.1093/cercor/bhh065     Document Type: Article

References (56)

1. Abeles M (1994) Firing rates and well-timed events. In: Models of neural networks II (Domany E, Schulten K, van Hemmen JL, eds), ch. 3. New York: Springer-Verlag.
2. Ariav G, Polsky A, Schiller J (2003) Submillisecond precision of the input/output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J Neurosci 23:7750-7758.
3. Berger T, Lüscher H-R (2003) Timing and precision of spike initiation in layer V pyramidal cells of the rat somatosensory cortex. Cereb Cortex 1:274-281.
4. Berger T, Larkum ME, Lüscher H-R (2001) A high Ih channel density in the distal apical dendrite of layer 5 pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol 85:855-868.
5. Budd JML (1998) Extrastriate feedback to primary visual cortex in primates: a quantitative analysis of connectivity. Proc R Soc Lond B Biol Sci 265:1037-1044.
6. Cauller LJ (1995) Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav Brain Res 71:163-70.
7. Cauller LJ, Connors BW (1994) Synaptic physiology of horizontal afferents to layer 1 in slices of rat SI neocortex. J Neurosci 14:751-762.
8. Cauller LJ, Clancy B, Connors BW (1998) Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J Comp Neurol 390:297-310.
9. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
10. Grill WE (1999) Functional implications of dendritic voltage-dependent conductances. J Physiol (Lond) 93:17-21.
11. Diamond ME (1995) Somatosensory thalamus of the rat. In: Cerebral cortex: the barrel cortex of rodents. Vol. 11, pp. 189-219. New York: Plenum Press.
12. Felleman DJ, van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
13. Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331.
14. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806-1814.
15. Körding K, König P (2000) Learning with two sites of synaptic integration. Network: Comp Neur Syst 11:1-15.
16. Lamme VAF, Super H, Spekreijse H (1998) Feedforward, horizontal, and feedback processing in the visual cortex. Curr Opin Neurobiol 8:529-535.
17. Larkum ME, Lüscher H-R (2002) Cortical gain control mechanism in the distal dendritic compartment of layer V pyramidal neurons. Soc Neurosci Abstr 345.1.
18. Larkum ME, Zhu JJ (2002) Signaling of layer 1 and whisker-evoked Ca2+ and Na+ APs in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J Neurosci 22:6991-7005.
19. Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-341.
20. Larkum ME, Zhu JJ, Sakmann B (2001) Dendritic mechanisms underlying the coupling of the dendritic with the axonal AP initiation zone of adult layer 5 pyramidal neurons. J Physiol (Lond) 533:447-466.
21. Lavenex P, Amaral, DG (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10:420-430.
22. Llinás RR, Leznik E, Urbano FJ (2002) Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci U S A 99:449-454.
23. London M, Schreibman A, Hausser M, Larkum ME, Segev I., (2002) The information efficacy of a synapse. Nat Neurosci 5:332-40.
24. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-6.
25. McAdams CJ, Maunsell HR (1999) Effects of attention on the reliability of individual neurons in monkey visual cortex. Neuron 23:765-773.
26. Oakley JC, Schwindt PC, Crill WE (2001) Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligandgated dendritic current to soma. J Neurophysiol 86:514-527.
27. Olson IR, Chun MM, Allison T (2001) Contextual guidance of attention. Human intracranial event-related potential evidence for feedback modulation in anatomically early, temporally late stages of visual processing. Brain 124:1417-1425.
28. Oviedo H, Reyes AD (2002) Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite. Nat Neurosci 5:261-266.
29. Oviedo H, Reyes AD (2003) Integrative properties of L5 pyramidal cells. Soc Neurosci Abstr 902.11.
30. Pike FG, Rhiannon MM, Olding AWA, Paulsen O (1999) Postsynaptic bursting is essential for 'Hebbian' induction of associative longterm potentiation at excitatory synapses in rat hippocampus. J Physiol (Lond) 518:571-576.
31. Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1:39-60.
32. Poirazi P, Brannon T, Mel BW (1993) Pyramidal neuron as two-layer neural network. Neuron 27:989-99.
33. Prescott SA, De Koninck Y (2003) Gain control of firing rate by shunting inhibition: roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci U S A 18:2076-2081.
34. Rail W (1964) Theoretical significance of dendritic trees for neuronal input-output relations. In: Neural theory and modeling (Reiss RF, ed.). Paolo Alto, CA: Stanford University Press.
35. Rhodes PA, Llinás RR (2001) Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex. J Physiol (Lond) 536:167-187.
36. Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3-20.
37. Rolls ET (2000) Hippocampo-cortical and cortico-cortical backprojections. Hippocampus 10:380-388.
38. Rudolph M, Destexhe A (2003) A fast-conducting, stochastic integrative mode for neocortical neurons in vivo. J Neurosci 23:2466-2476.
39. Saunas E, Sejnowski TJ (2001) Gain modulation in the central nervous system: where behavior, neurophysiology, and computation meet. Neuroscientist 7:430-440.
40. Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to the distal apical dendrites of rat neocortical pyramidal neurons. J Physiol (Lond) 505:605-616.
41. Schwindt W, Crill WE (1995) Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74:2220-2224.
42. Shadlen MN, Newsome WT (1994) Noise, neural code and cortical organization. Curr Opin Neurobiol 4:569-579.
43. Shao ZW, Burkhalter A (1996) Different balance of excitation and inhibition in forward and feedback circuits of rat visual cortex. J Neurosci 16:7353-7365.
44. Shulman GL, Ollinger JM, Akbudak E, Conturo TE, Snyder AZ, Petersen SE, Corbetta M (1999) Areas involved in encoding and applying directional expectations to moving objects. J Neurosci 19:9480-9496.
45. Siegel M, Körding KP, König P (2000) Integrating top-down and bottom-up sensory processing by somato-dendritic interactions. J Comp Neurosci 8:161-173.
46. Snider RK, Kabara JF, Roig BR, Bonds AB (1998) Burst firing and modulation of functional connectivity in cat striate cortex. J Neurophysiol 80:730-744.
47. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-350.
48. Softky WR (1994) Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58:13-41.
49. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
50. Stuart GJ, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium-channels in neocortical pyramidal neurons. Neuron 15:1065-1076.
51. Stuart GJ, Schiller J, Sakmann B (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol (Lond) 505:617-632.
52. Stuart GJ, Häusser M (2001) Dendritic coincidence detection of EPSPs and action potentials. Nat Neurosci 4:63-71.
53. Tuckwell HC (1988) Introduction to theoretical neurobiology. Cambridge: Cambridge University Press.
54. Van Vreeskijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726.
55. Williams SR, Stuart GJ (1999) Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol (Lond) 521:467-482.
56. Williams SR, Stuart GJ (2002) Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295:1907-1910.