The development of voltage-sensitive dyes (VSD) and fast optical imaging techniques have brought us a new tool for examining spatiotemporal patterns of population neuronal activity in the neocortex. Propagating waves have been observed during almost every type of cortical processing examined by VSD imaging or electrode arrays. These waves provide subthreshold depolarization to individual neurons and increase their spiking probability. Therefore, the propagation of the waves sets up a spatiotemporal framework for increased excitability in neuronal populations, which can help to determine when and where the neurons are likely to fire. In this review, first discussed is propagating waves observed in various systems and possible mechanisms for generating and sustaining these waves. Then discussed are wave dynamics as an emergent behavior of the population activity that can, in turn, influence the activity of individual neurons. The functions of spontaneous and sensory-evoked waves remain to be explored. An important next step will be to examine the interaction between dynamics of propagating waves and functions in the cortex, and to verify if cortical processing can be modified when these waves are altered. NEUROSCIENTIST 14(5):487—502, 2008. DOI: 10.1177/1073858408317066
Albowitz B., Kuhnt U.1995. Epileptiform activity in the guinea-pig neocortical slice spreads preferentially along supragranular layers-recordings with voltage-sensitive dyes. Eur J Neurosci7:1273-84.
2.
Anderson WW, Lewis DV, Swartzwelder HS, Wilson WA1986. Magnesium-free medium activates seizure-like events in the rat hippocampal slice. Brain Res398:215-9.
3.
Arieli A., Shoham D., Hildesheim R., Grinvald A.1995. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. J Neurophysiol73:2072-93.
4.
Arieli A., Sterkin A., Grinvald A., Aertsen A.1996. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science273:1868-71.
5.
Bai L., Huang X., Yang Q., Wu JY2006. Spatiotemporal patterns of an evoked network oscillation in neocortical slices: coupled local oscillators. J Neurophysiol96:2528-38.
6.
Bao W., Wu JY2003. Propagating wave and irregular dynamics: spatiotemporal patterns of cholinergic theta oscillations in neocortex in vitro. J Neurophysiol90:333-41.
7.
Benucci A., Frazor RA, Carandini M.2007. Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron55:103-17.
8.
Buhl EH, Tamas G., Fisahn A.1998. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol513 (Pt 1):117-26.
9.
Chen Y., Geisler WS, Seidemann E.2006. Optimal decoding of correlated neural population responses in the primate visual cortex. Nat Neurosci9:1412-20.
10.
Chervin RD, Pierce PA, Connors BW1988. Periodicity and directionality in the propagation of epileptiform discharges across neocortex. J Neurophysiol60:1695-713.
11.
Civillico EF, Contreras D.2005. Comparison of responses to electrical stimulation and whisker deflection using two different voltage-sensitive dyes in mouse barrel cortex in vivo. J Membr Biol208:171-82.
12.
Cohen LB, Keynes RD, Hille B.1968. Light scattering and birefringence changes during nerve activity. Nature218:438-41.
13.
Delaney KR, Gelperin A., Fee MS, Flores JA, Gervais R., Tank DW, and others. 1994. Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc Natl Acad Sci U S A91:669-73.
14.
Demir R., Haberly LB, Jackson MB1998. Voltage imaging of epileptiform activity in slices from rat piriform cortex: onset and propagation. J Neurophysiol80:2727-42.
15.
Derdikman D., Hildesheim R., Ahissar E., Arieli A., Grinvald A.2003. Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J Neurosci23:3100-5.
16.
Destexhe A., Rudolph M., Pare D.2003. The high-conductance state of neocortical neurons in vivo . Nat Rev Neurosci4:739-51.
17.
Douglas R., Markram H., Martin K.2004. Neocortex. In: Shepherd GM, editor. The synaptic organization of the brain . 5th ed. New York: Oxford University Press. p 499-558.
18.
Eeckman FH, Freeman WJ1990. Correlations between unit firing and EEG in the rat olfactory system. Brain Res528:238-44.
19.
Eriksson D., Roland P.2006. Feed-forward, feedback and lateral interactions in membrane potentials and spike trains from the visual cortex in vivo. J Physiol Paris100:100-9.
20.
Ermentrout GB, Kleinfeld D.2001. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron29(1):33-44.
21.
Ferezou I., Bolea S., Petersen CC2006. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron50:617-29.
22.
Ferezou I., Haiss F., Gentet LJ, Aronoff R., Weber B., Petersen CC2007. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron56:907-23.
23.
Fisahn A., Pike FG, Buhl EH, Paulsen O.1998. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature394:186-9.
24.
Freeman WJ1978. Spatial properties of an EEG event in the olfactory bulb and cortex. Electroencephalogr Clin Neurophysiol44:586-605.
25.
Frostig RD2006. Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr Opin Neurobiol16:445-50.
26.
Gelperin A., Tank DW1990. Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature345:437-40.
27.
Golomb D., Amitai Y.1997. Propagating neuronal discharges in neocortical slices: computational and experimental study. J Neurophysiol78:1199-211.
28.
Golomb D., Ermentrout GB2002. Slow excitation supports propagation of slow pulses in networks of excitatory and inhibitory populations. Phys Rev E Stat Nonlin Soft Matter Phys65(6 Pt 1):061911.
29.
Grinvald A., Anglister L., Freeman JA, Hildesheim R., Manker A.1984. Real-time optical imaging of naturally evoked electrical activity in intact frog brain. Nature308:848-50.
30.
Grinvald A., Hildesheim R.2004. VSDI: a new era in functional imaging of cortical dynamics . Nat Rev Neurosci5:874-85.
31.
Grinvald A., Lieke EE, Frostig RD, Hildesheim R.1994. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci14(5 Pt 1):2545-68.
32.
Haydon PG2001. GLIA: listening and talking to the synapse. Nat Rev Neurosci2:185-93.
33.
Huang X., Troy WC, Yang Q., Ma H., Laing CR, Schiff SJ, and others. 2004. Spiral waves in disinhibited mammalian neocortex. J Neurosci24:9897-902.
34.
Hubel DH, Wiesel TN1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol160:106-54.
35.
Jancke D., Chavane F., Naaman S., Grinvald A.2004. Imaging cortical correlates of illusion in early visual cortex. Nature428:423-6.
36.
Kalatsky VA, Stryker MP2003. New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron38:529-45.
37.
Katz LC, Shatz CJ1996. Synaptic activity and the construction of cortical circuits . Science274:1133-8.
38.
Kenet T., Bibitchkov D., Tsodyks M., Grinvald A., Arieli A.2003. Spontaneously emerging cortical representations of visual attributes. Nature425:954-6.
39.
Kim U., Bal T., McCormick DA1995. Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. J Neurophysiol74:1301-23.
40.
Kleinfeld D., Delaney KR1996. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes . J Comp Neurol375:89-108.
41.
Lam YW, Cohen LB, Wachowiak M., Zochowski MR2000. Odors elicit three different oscillations in the turtle olfactory bulb. J Neurosci20:749-62.
42.
Lampl I., Reichova I., Ferster D.1999. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron22:361-74.
43.
Lippert MT, Takagaki K., Xu W., Huang X., Wu JY2007. Methods for voltage-sensitive dye imaging of rat cortical activity with high signal-to-noise ratio. J Neurophysiol98:502-12.
44.
London JA, Cohen LB, Wu JY1989. Optical recordings of the cortical response to whisker stimulation before and after the addition of an epileptogenic agent . J Neurosci9:2182-90.
45.
Lukatch HS, MacIver MB1997. Physiology, pharmacology, and topography of cholinergic neocortical oscillations in vitro. J Neurophysiol77:2427-45.
46.
Luhmann HJ, Prince DA1990. Transient expression of polysynaptic NMDA receptor-mediated activity during neocortical development. Neurosci Lett111:109-15.
47.
Mann EO, Suckling JM, Hajos N., Greenfield SA, Paulsen O.2005. Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron45:105-17.
48.
Metherate R., Cruikshank SJ1999. Thalamocortical inputs trigger a propagating envelope of gamma-band activity in auditory cortex in vitro. Exp Brain Res126:160-74.
49.
Miles R., Traub RD, Wong RK1988. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J Neurophysiol60:1481-96.
50.
Momose-Sato Y., Sato K., Kinoshita M.2007. Spontaneous depolarization waves of multiple origins in the embryonic rat CNS. Eur J Neurosci25:929-44.
51.
Moore CI, Nelson SB1998. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol80:2882-92.
52.
Nishimura M., Shirasawa H., Kaizo H., Song WJ2007. New field with tonotopic organization in guinea pig auditory cortex. J Neurophysiol97:927-32.
53.
Orbach HS, Cohen LB1983. Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system. J Neurosci3:2251-62.
54.
Orbach HS, Cohen LB, Grinvald A.1985. Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci5:1886-95.
55.
Petersen CC2007. The functional organization of the barrel cortex . Neuron56:339-55.
56.
Petersen CC, Grinvald A., Sakmann B.2003. Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J Neurosci23:1298-309.
57.
Petersen CC, Hahn TT, Mehta M., Grinvald A., Sakmann B.2003. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A100:13638-43.
58.
Pinto DJ, Ermentrout GB2001. Spatially structured activity in synaptically coupled neuronal networks: I. Traveling fronts and pulses. SIAM Appl Math62:206-225.
59.
Powell TP, Mountcastle VB1959. Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull Johns Hopkins Hosp105:133-62.
60.
Prechtl JC, Cohen LB, Pesaran B., Mitra PP, Kleinfeld D.1997. Visual stimuli induce waves of electrical activity in turtle cortex. Proc Natl Acad Sci U S A94:7621-6.
61.
Roland PE, Hanazawa A., Undeman C., Eriksson D., Tompa T., Nakamura H., and others. 2006. Cortical feedback depolarization waves: a mechanism of top-down influence on early visual areas. Proc Natl Acad Sci U S A103:12586-91.
62.
Ross WN, Salzberg BM, Cohen LB, Grinvald A., Davila HV, Waggoner AS, and others. 1977. Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential. J Membr Biol33:141-83.
63.
Rubino D., Robbins KA, Hatsopoulos NG2006. Propagating waves mediate information transfer in the motor cortex. Nat Neurosci9:1549-57.
64.
Schiff SJ, Huang X., Wu JY2007. Dynamical evolution of spatiotemporal patterns in mammalian middle cortex. Phys Rev Lett98:178102.
65.
Senseman DM, Robbins KA1999. Modal behavior of cortical neural networks during visual processing. J Neurosci19:RC3.
66.
Sharon D., Grinvald A.2002. Dynamics and constancy in cortical spatiotemporal patterns of orientation processing. Science295:512-5.
67.
Sharon D., Jancke D., Chavane F., Na'aman S., Grinvald A.2007. Cortical response field dynamics in cat visual cortex . Cereb Cortex17:2866-77.
68.
Shoham D., Glaser DE, Arieli A., Kenet T., Wijnbergen C., Toledo Y., and others. 1999. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron24(4):791-802.
69.
Shu Y., Hasenstaub A., McCormick DA2003. Turning on and off recurrent balanced cortical activity . Nature423:288-93.
70.
Silva LR, Amitai Y., Connors BW1991. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science251:432-5.
71.
Slovin H., Arieli A., Hildesheim R., Grinvald A.2002. Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. J Neurophysiol88:3421-38.
72.
Song WJ, Kawaguchi H., Totoki S., Inoue Y., Katura T., Maeda S., and others. 2006. Cortical intrinsic circuits can support activity propagation through an isofrequency strip of the guinea pig primary auditory cortex. Cereb Cortex16:718-29.
73.
Steriade M., McCormick DA, Sejnowski TJ1993. Thalamocortical oscillations in the sleeping and aroused brain. Science262:679-85.
74.
Takagaki K., Zhang C., Wu JY, Lippert MT2008. Crossmodal propagation of sensory-evoked and spontaneous activity in the rat neocortex. Neurosci Lett431:191-6.
75.
Towers SK, LeBeau FE, Gloveli T., Traub RD, Whittington MA, Buhl EH2002. Fast network oscillations in the rat dentate gyrus in vitro. J Neurophysiol87:1165-8. Tsau Y., Guan L., Wu JY1998. Initiation of spontaneous epileptiform activity in the neocortical slice. J Neurophysiol80:978-82.
76.
Webb SE, Miller AL2003. Calcium signalling during embryonic development . Nat Rev Mol Cell Biol4:539-51.
77.
Whittington MA, Traub RD, Jefferys JG1995. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature373:612-5. Wilson HR, Cowan JD1972. Excitatory and inhibitory interactions in localized populations of model neurons . Biophys J12:1-24.
78.
Wilson HR, Cowan JD1973. A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik13:55-80.
79.
Winfree AT2001. The geometry of biological time. New York: Springer-Verlag.
80.
Witte RS, Rousche PJ, Kipke DR2007. Fast wave propagation in auditory cortex of an awake cat using a chronic microelectrode array. J Neural Eng4:68-78.
81.
Wong RO1999. Retinal waves and visual system development. Annu Rev Neurosci22:29-47.
82.
Woolsey C., Marshall WH, Bard P.1942. Representation of cutaneous tactile sensibility in the cerebral cortex of the monkey as indicated by evoked potentials. Bull Johns Hopkins Hosp70:399-441.
83.
Woolsey TA, Van der Loos H.1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res17:205-42.
84.
Wu JY, Guan L., Bai L., Yang Q.2001. Spatiotemporal properties of an evoked population activity in rat sensory cortical slices. J Neurophysiol86:2461-74.
85.
Wu JY, Guan L., Tsau Y.1999. Propagating activation during oscillations and evoked responses in neocortical slices. J Neurosci19:5005-15.
86.
Xu W., Huang X., Takagaki K., Wu JY2007. Compression and reflection of visually evoked cortical waves. Neuron55:119-29.
