Attention-dependent reductions in burstiness and action-potential height in macaque area V4

Nature Neuroscience

Volumn 16, Issue 8, 2013, Pages 1125-1131

  Anderson, Emily B ^a,b   Mitchell, Jude F ^a   Reynolds, John H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; ATTENTION; CONDUCTANCE; CONTROLLED STUDY; MACACA; MALE; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTIVE FIELD; VISUAL AREA V4;

ACTION POTENTIALS; ANIMALS; ATTENTION; CUES; INTERNEURONS; ION TRANSPORT; MACACA; MALE; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; POTASSIUM CHANNELS, VOLTAGE-GATED; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL CELLS; VISUAL CORTEX;

EID: 84880924261     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3463     Document Type: Article

References (50)

1. Krahe, R. & Gabbiani, F. Burst firing in sensory systems. Nat. Rev. Neurosci. 5, 13-23 (2004). (Pubitemid 38076180)
2. Sherman, S.M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122-126 (2001).
3. Cattaneo, A., Maffei, L. & Morrone, C. Patterns in the discharge of simple and complex visual cortical cells. Proc. R. Soc. Lond. B Biol. Sci. 212, 279-297 (1981). (Pubitemid 11001819)
4. Samonds, J.M. & Bonds, A.B. From another angle: differences in cortical coding between fine and coarse discrimination of orientation. J. Neurophysiol. 91, 1193-1202 (2004). (Pubitemid 38250403)
5. Shih, J.Y., Atencio, C.A. & Schreiner, C.E. Improved stimulus representation by short interspike intervals in primary auditory cortex. J. Neurophysiol. 105, 1908-1917 (2011).
6. Reich, D.S., Mechler, F., Purpura, K.P. & Victor, J.D. Interspike intervals, receptive fields, and information encoding in primary visual cortex. J. Neurosci. 20, 1964-1974 (2000). (Pubitemid 30220393)
7. Izhikevich, E.M., Desai, N.S., Walcott, E.C. & Hoppensteadt, F.C. Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci. 26, 161-167 (2003). (Pubitemid 36183678)
8. Caporale, N. & Dan, Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25-46 (2008).
9. Sjöström, P.J., Rancz, E.A., Roth, A. & Häusser, M. Dendritic excitability and synaptic plasticity. Physiol. Rev. 88, 769-840 (2008). (Pubitemid 351520092)
10. De Weerd, P., Peralta, M.R. III, Desimone, R. & Ungerleider, L.G. Loss of attentional stimulus selection after extrastriate cortical lesions in macaques. Nat. Neurosci. 2, 753-758 (1999). (Pubitemid 30491198)
11. Reynolds, J.H. & Heeger, D.J. The normalization model of attention. Neuron 61, 168-185 (2009).
12. Mitchell, J.F., Sundberg, K.A. & Reynolds, J.H. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55, 131-141 (2007). (Pubitemid 46990821)
13. Brumberg, J.C., Nowak, L.G. & McCormick, D.A. Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J. Neurosci. 20, 4829-4843 (2000). (Pubitemid 30421686)
14. Nowak, L.G., Azouz, R., Sanchez-Vives, M.V., Gray, C.M. & McCormick, D.A. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J. Neurophysiol. 89, 1541-1566 (2003). (Pubitemid 36323999)
15. Vigneswaran, G., Kraskov, A. & Lemon, R.N. Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J. Neurosci. 31, 14235-14242 (2011).
16. Anderson, E.B., Mitchell, J.F. & Reynolds, J.H. Attentional modulation of firing rate varies with burstiness across putative pyramidal neurons in macaque visual Area V4. J. Neurosci. 31, 10983-10992 (2011).
17. Mitchell, J.F., Sundberg, K.A. & Reynolds, J.H. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63, 879-888 (2009).
18. Arieli, A., Sterkin, A., Grinvald, A. & Aertsen, A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868-1871 (1996). (Pubitemid 26322498)
19. Smith, M.A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591-12603 (2008).
20. Wang, Z. & McCormick, D.A. Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J. Neurosci. 13, 2199-2216 (1993). (Pubitemid 23113427)
21. Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969-1985 (2001). (Pubitemid 32440676)
22. Golomb, D., Cuiyong, Y. & Yaari, Y. Contribution of persistent Na+ current and M-type K+ current to somatic bursting in CA1 pyramidal cells: combined experimental and modeling study. J. Neurophysiol. 96, 1912-1926 (2006). (Pubitemid 44527446)
23. Destexhe, A., Rudolph, M., Fellous, J.M. & Sejnowski, T.J. Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107, 13-24 (2001). (Pubitemid 34020681)
24. Reynolds, J.H., Chelazzi, L. & Desimone, R. Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4. J. Neurosci. 19, 1736-1753 (1999). (Pubitemid 29094192)
25. Yue, C. & Yaari, Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 24, 4614-4624 (2004). (Pubitemid 38656617)
26. Colbert, C.M., Magee, J.C., Hoffman, D.A. & Johnston, D. Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 17, 6512-6521 (1997). (Pubitemid 27366603)
27. Jung, H.-Y., Mickus, T. & Spruston, N. Prolonged sodium channel inactivation contributes to dendritic action potential attenuation in hippocampal pyramidal neurons. J. Neurosci. 17, 6639-6646 (1997). (Pubitemid 27366616)
28. Martina, M. & Jonas, P. Functional differences in Na+ channel gating between fast-spiking interneurones and principal neurones of rat hippocampus. J. Physiol. (Lond.) 505, 593-603 (1997). (Pubitemid 28022361)
29. Bean, B.P. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8, 451-465 (2007). (Pubitemid 46789230)
30. McCormick, D.A., Connors, B.W., Lighthall, J.W. & Prince, D.A. Comparative electrophysiology of pyramidal and sparsely spiny neurons of the neocortex. J. Neurophysiol. 54, 782-806 (1985). (Pubitemid 16253719)
31. Gonzàlez-Burgos, G., Krimer, L.S., Povysheva, N.V., Barrionuevo, G. & Lewis, D.A. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J. Neurophysiol. 93, 942-953 (2005).
32. Carter, B.C. & Bean, B.P. Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast spiking neurons. Neuron 64, 898-909 (2009).
33. de Polavieja, G.G., Harsch, A., Kleppe, I., Robinson, H.P.C. & Juusola, M. Stimulus history reliably shapes action potential waveforms of cortical neurons. J. Neurosci. 25, 5657-5665 (2005). (Pubitemid 40800658)
34. McAdams, C.J. & Maunsell, J.H. Effects of attention on orientation tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431-441 (1999). (Pubitemid 29028982)
35. Harris, K.D. & Thiele, A. Cortical state and attention. Nat. Rev. Neurosci. 12, 509-523 (2011).
36. Noudoost, B., Chang, M.H., Steinmetz, N.A. & Moore, T. Top-down control of visual attention. Curr. Opin. Neurobiol. 20, 183-190 (2010).
37. Pinsky, P.F. & Rinzel, J. Intrinsic and network rhythmogenesis in a reduced traub model for CA3 neurons. J. Comp. Neurosci. 1, 39-60 (1994).
38. Mainen, Z.F. & Sejnowski, T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363-366 (1996). (Pubitemid 26260465)
39. Kepecs, A. & Wang, X.-J. Analysis of complex bursting in cortical pyramidal neuron models. Neurocomputing 32, 181-187 (2000). (Pubitemid 30459718)
40. Matsumura, M., Chen, D., Sawaguchi, T., Kubota, K. & Fetz, E.E. Synaptic interactions between primate precentral cortex neurons revealed by spike-triggered averaging of intracellular membrane potentials in vivo. J. Neurosci. 16, 7757-7767 (1996). (Pubitemid 26389714)
41. Anderson, J.S., Carandini, M. & Ferster, X. Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926 (2000). (Pubitemid 30655612)
42. Gold, C., Henze, D.A., Koch, C. & Buzsáki, G. On the origin of the extracellular action potential waveform: a modeling study. J. Neurophysiol. 95, 3113-3128 (2006).
43. Henze, D.A. et al. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 84, 390-400 (2000). (Pubitemid 30490059)
44. Harris, K.D. et al. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141-149 (2001). (Pubitemid 32995896)
45. Quirk, M.C., Blum, K.E. & Wilson, M.A. Experience-dependent changes in extracellular spike amplitude may reflect regulation of dendritic action potential back-propagation in rat hippocampal pyramidal cells. J. Neurosci. 21, 240-248 (2001). (Pubitemid 32098747)
46. Ringach, D.L., Hawken, M.J. & Shapley, R. Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281-284 (1997). (Pubitemid 27220762)
47. Pylyshyn, Z.W. & Storm, R.W. Tracking multiple independent targets: evidence for a parallel tracking mechanism. Spat. Vis. 3, 179-197 (1988).
48. Cavanagh, P. & Alvarez, G.A. Tracking multiple targets with multifocal attention. Trends Cogn. Sci. 9, 349-354 (2005). (Pubitemid 40910334)
49. Barth, P. et al. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J. Neurophysiol. 92, 600-608 (2004).
50. Aracri, P. et al. Layer-specific properties of the persistent sodium current in sensorimotor cortex. J. Neurophysiol. 95, 3460-3468 (2006). (Pubitemid 43846155)