Fast Propagating Waves within the Rodent Auditory Cortex

Central processing of acoustic signals is assumed to take place ina stereotypical spatial and temporal pattern involving differentfields of auditory cortex. So far, cortical propagating wavesrepresenting such patterns have mainly been demonstrated byoptical imaging, repeatedly in the visual and somatosensory cortex.In this study, the surface of rat auditory cortex was mapped byrecording local field potentials (LFPs) in response to a broadbandacoustic stimulus. From the peak amplitudes of LFPs, corticalactivation maps were constructed over 4 cortical auditory fields.Whereas response onset had same latencies across primary auditoryfield (A1), anterior auditory field (AAF), and ventral auditory field andlonger latencies in posterior auditory field, activation maps revealeda reproducible wavelike pattern of activity propagating for ~45 mspoststimulus through all cortical fields. The movement observedstarted with 2 waves within the primary auditory fields A1 and AAFmoving from ventral to dorsal followed by a motion from rostral tocaudal, passing continuously through higher-order fields. The patternof propagating waves was well reproducible and showed only minorchanges if different anesthetics were used. The results question theclassical ‘‘hierarchical’’ model of cortical areas and demonstrate thatthe different fields process incoming information as a functional unit.Keywords: anesthesia, cortical hierarchy, cortical organization,spatiotemporal pattern, traveling waveIntroductionThe brain represents features of sensory stimuli by the locationof maximal excitation and by temporal features of neuronalresponses. Provided that these 2 organizational principles act incoordinated fashion, they should generate a complex spatio-temporalpatternofevokedactivity.Indeed,propagatingcorticalwaveshavebeenreportedinthevisual(Prechtletal.1997,2000;Senseman and Robbins 1999; Sharon and Grinvald 2002; Rolandet al. 2006; Benucci et al. 2007; Xu et al. 2007), somatosensory(Derdikman et al. 2003; Petersen et al. 2003), and motor cortex(Rubinoetal.2006)aswellasintheolfactorybulb(Delaneyetal.1994). Propagating waves result when groups of neuronssequentially depolarize and hyperpolarize with small delays;the activity ‘‘travels’’ through the cortex according to the orderandthedegreeofactivationofareas.Thevastmajorityofreportson cortical propagating waves applied optical imaging methods(Delaney et al. 1994; Prechtl et al. 1997; Sharon and Grinvald2002; Derdikman et al. 2003; Petersen et al. 2003; Roland et al.2006; Benucci et al. 2007; Xu et al. 2007).In the auditory system, evoked propagating waves in thetimescale of hundreds of milliseconds have been described andshown to propagate mainly within the isofrequency stripe infield primary auditory field (A1) (Bakin et al. 1996; Hess andScheich 1996; Tsytsarev and Tanaka 2002; Tsytsarev et al.2004). Using voltage-sensitive dyes, a cortical wave in thetimescale of dozens of milliseconds was observed, againpropagating within the isofrequency stripe (Song et al. 2006).This spread of activity has an anatomical correlate as thalamicafferents spread within the isofrequency stripe in a patchypattern (Velenovsky et al. 2003; McMullen et al. 2005). On theother hand, both thalamocortical as well as corticocorticalprojections involve a significant extent of cortical tissueorthogonal to the isofrequency stripe (Lee and Winer 2008a,2008b). Most likely, the propagation within the isofrequencyband has been the consequence of pure tone stimulation usedin previous studies, selected in the attempt to demonstratecochleotopic cortical organization of the cortex and by that toverify the usefulness of optical imaging methods.Optical imaging methods, especially intrinsic optical signals,have a high spatial resolution but hold the disadvantage ofbeing insensitive to rapid changes in the temporal domain(Nelkenetal.2008;fordependenceonwavelength,seeTsytsarevet al. 2008), thus providing temporally smoothed patterns of fastcortical activity. Voltage-sensitive dyes, although essentially toxicfor neurons, allow determining faster changes of neuronalactivity (Song et al. 2006; Tsytsarev et al. 2008). Differences intiming in the range of few milliseconds appear cardinal incortical representation of the sensory world (Goure´vitch andEggermont 2007; Wei et al. 2008) and possibly in differentiatingauditory objects (Nelken 2004). Consequently, direct electro-physiological investigations of propagating waves are required toinvestigate the true temporal scale over which they occur. Incochlear-implanted cats, a first electrophysiological study indeedobserved a complex pattern of waves and ‘‘reflection’’ waves infields A1 and anterior auditory field (AAF) evoked by electricalcochlear stimulation (Kral et al. 2009).The present study demonstrates that evoked propagatingwaves can be observed also with acoustic stimuli, that theycover the whole auditory cortex, and that they travel in 2directions: within A1 first dorsally, then also caudally andventrally, and within AAF first dorsally, then ventrorostrally.Both activation fronts (from A1 and AAF) unify in passingthrough ventral auditory field (VAF) and end in posteriorauditory field (PAF). To minimize a possible contamination ofthe wave by the anesthetics, 3 different anesthetic conditionswith differently acting anesthetics were compared: 2 volatileanesthetics (isoflurane with and without nitrous oxide) and 1nonvolatile anesthetic agent (ketamine). The study demon-strates that despite specific effects of the different anesthetics,cortical propagating waves constitute a stable phenomenon.The propagating waves demonstrated in this investigationfurther allow drawing conclusions about the hierarchical orderof the cortical sensory areas in rat auditory cortex.