Cortical interference effects in the cocktail party problem

Transcription

1 7 Nture Pulishing Group Cortil interferene effets in the oktil prty prolem Rjiv Nryn 1,, Virgini Best 1,3, Erol Ozmerl 1,3, Elizeth MCline 1,, Mihel Dent, Brr Shinn-Cunninghm 1 3 & Kml Sen 1, Humns nd nimls must often disriminte etween omplex nturl sounds in the presene of ompeting sounds (mskers). Although the uditory ortex is thought to e importnt in this tsk, the impt of mskers on ortil disrimintion remins poorly understood. We exmined neurl responses in zer finh (Teniopygi guttt) field L (homologous to primry uditory ortex) to trget irdsongs tht were emedded in three different mskers (rodnd noise, modulted noise nd irdsong horus). We found two distint forms of interferene in the neurl responses: the ddition of spurious spikes ourring primrily during the silent gps etween song syllles nd the suppression of informtive spikes ourring primrily during the syllles. Both effets systemtilly degrded neurl disrimintion s the trget intensity deresed reltive to tht of the msker. The ehviorl performne of songirds degrded in prllel mnner. Our results identify neurl interferene tht ould explin the pereptul interferene t the hert of the oktil prty prolem. In everydy settings, our ers re onstntly omrded y mixture of sounds oming from multiple, simultneous soures. Mny speies of nimls, inluding irds 1,frogs nd mmmls 3, re dept t nlyzing the ousti mixture to determine whih sound soures re present, n ility tht is importnt for proretion nd survivl. In humns, the prolem of identifying speeh in kground of ompeting sounds is often desried s the oktil prty prolem (CPP) 3,. The CPP is espeilly hllenging for hering-impired listeners nd rtifiil speeh-reognition systems 5 7. Norml-hering listeners lso hve reltive diffiulty solving this prolem under ertin onditions; for exmple, when the trget nd mskers re spetro-temporlly similr nd/or sptilly oloted 8,9. Exmining neurl responses to nturl stimuli in the presene of mskers my revel interferene tht ould explin diffiulties in pereptul disrimintion under dverse onditions. The uditory ortex is thought to e ritilly involved in proessing omplex nturl sounds 13. Although rodnd noise hs een shown to produe nonliner effets on ortil responses to nturl sounds, the impt of spetro-temporlly omplex mskers on ortil disrimintion remins unler. Here we studied the effets of different mskers on ortil disrimintion in the songird, model system tht shows similrities to humns in the ontext of vol ommunition 1.Songirdsrettrtivefor studying the CPP euse they ommunite using omplex vol ommunition sounds in omplex ousti environments (for exmple, in thepreseneofmnyotherirdsvolizinginthekground 1 ). In this study, we reorded neurl responses from zer finh field L, the vin homolog of the mmmlin uditory ortex, whih is thought to e involved in the proessing of onspeifi songs 15,1.Inpreviouswork,we hve shown tht the responses of single units in field L provide suffiient informtion to disriminte etween onspeifi songs 11,13.Herewe extended this work to exmine how response ptterns re ffeted y different kinds of simultneous mskers tht use distint ptterns of ehviorl disruption in humn listeners 17. Our im ws to identify how the different mskers ffet neurl responses nd to determine how this interferene trnsltes into hnges in neurl disrimintion. RESULTS Neurl responses to trgets nd mskers We exmined neurl responses to trget songs presented in quiet or emedded in three different mskers: rodnd noise (lso referred to simply s noise), modulted noise nd irdsong horus (see Fig. 1 nd Methods). Trget intensity ws vried systemtilly (with the msker held t fixed intensity) to give five different trget-to-msker rtios (TMRs). In generl, the neurl sites showed strong, phse-loked responses to individul syllles of the trget (Fig. ). Response sensitivity to msked trgets vried ross sites, ut response ptterns devited further from the unmsked responses s the TMR deresed (Fig. ). We oserved two types of neurl interferene. There were dditions of spikes (oserved prtiulrly during the gps etween the trget song syllles) nd suppression of spikes (oserved prtiulrly during the syllles of the trget). The reltive ontriutions of these two effets depended on the prtiulr site, the type of msker nd the TMR. Spike suppression ws prtiulrly visile t low TMRs, wheres spike dditions ppered to e lrgely independent of TMR. 1 Hering Reserh Center nd Deprtment of Biomedil Engineering, Boston University, Cummington Street, Boston, Msshusetts 15, USA. 3 Deprtment of Cognitive nd Neurl Systems, Boston University, 77 Beon Street, Boston, Msshusetts 15, USA. Deprtment of Psyhology, University t Bufflo, The Stte University of New York, Prk Hll Room, Bufflo, New York 1-1, USA. Correspondene should e ddressed to K.S. (kmlsen@u.edu). Reeived 9 August; epted Otoer; pulished online 11 Novemer 7; doi:.38/nn9 NATURE NEUROSCIENCE VOLUME [ NUMBER 1 [ DECEMBER 7 11

2 7 Nture Pulishing Group d Time (ms) Trget Brodnd noise Modulted noise Although unmsked responses to the trgets were otined for ll sites t single intensity ( db reltive to the fixed msker intensity), responsesforthefullrngeoftrgetintensitiesusedinthemskedtrilswere otined from suset of sites. In this suset, we found tht the rtes were reltively unhnged with vrying trget intensity (Fig. ). This suggests tht the hnges in firing-rte ptterns tht were oserved in the msked onditions (spike suppression nd spike dditions) were result ofthepreseneofthemskerndnotthesoluteintensityofthetrget. To quntify the interferene ttriutle to dditions nd deletions of spikes, trget stimuli were segmented into syllles nd temporl gps, nd men firing rtes in these regions were ompred for responses to unmsked nd msked stimuli t the -db TMR ross Figure Neurl responses to trgets in the presene of mskers. () The sound pressure wveform of trget s funtion of time. () Responses of two representtive sites to the trget shown in, emedded in three mskers. For eh site, the top three pnels depit olor-oded men firing rtes of the responses to the sme trget in noise, modulted noise nd horus, respetively. Trget intensity ws vried systemtilly with the msker held t fixed intensity to give five different TMRs. In eh pnel, the responses re rrnged in deresing TMR order (from top to ottom, + db to db). The lst pnel shows the men firing rte response of eh site to tokens of the trget presented lone, s funtion of deresing trget intensity. The olor-oded rtes re normlized to the pek rte of the response to the trget in the unmsked ondition t -db TMR. () The men differenes in firing rte (msked unmsked response) oth within nd etween trget syllles t -db TMR (men ± s.e.m., n ¼ 9). Positive differenes in the men firing rte reflet dominne of spike dditions nd negtive differenes reflet dominne of spike suppression. Within syllles, sites showed redution in men firing rte in horus nd noise, wheres 3 sites showed n inrese in firing rte in modulted noise. Between syllles, n inrese in firing rte ws oserved in, 8 nd 3 sites for horus, modulted noise nd noise, respetively. Noise Modulted noise Clen 5 5 Clen Modulted Noise noise Figure 1 Trget nd msker stimuli. ( d) Exemplr spetrogrms of trget song () nd eh of the three types of mskers: rodnd noise (, stedystte noise with spetrl ontent mthing the horus) modulted noise (, rodnd noise multiplied y the envelope of horus), nd horus (d, rndom omintion of three non-trget irdsongs). ll sites (see Fig. nd Methods). Overll, within syllles, the men firing rte ws redued y noise nd horus mskers, ut ws inresed y the modulted noise msker. Chnges in within-syllle firing rtes were signifintly different for the different msker types (F,13 ¼., P o.1, one-wy repeted mesures ANOVA) nd Tukey post ho omprisons indited tht there were signifint differenes etween modulted noise nd noise (P o.1) nd etween modulted noise nd horus (P o.1), ut not etween noise nd horus (P ¼.93). Between syllles, the men firing rte ws inresed in the presene of the different mskers. Chnges in etweensyllle firing rtes were signifintly different ross msker types (F,13 ¼ 39.75, P o.1, one-wy repeted mesures ANOVA) nd Tukey post ho omprisons indited tht the effets of the three mskers were ll signifintly different from eh other (P o.1). We evluted the effet of TMR on the differenes in firing rte within nd etween trget syllles mong different mskers in the suset of sites where unmsked responses to the trgets were reorded for ll of the trget intensities (Supplementry Fig. 1 online). Within trget syllles, the mskers generlly used suppression; however, modulted noise used spike dditions t TMRs r db. Between trget syllles, ll mskers used spike dditions t ll TMRs. Neurl disrimintion in the presene of msker We quntified neurl disrimintion using metri-sed spike-trin lssifition sheme (see Methods). The ury of lssifying the trget songs emedded in the three msker types t different TMRs Site 1 Site 7 Time (ms) TMR Trget intensity Rte (msked len) spikes s 1 7 Within syllle Noise Modulted noise Between syllle 1 VOLUME [ NUMBER 1 [ DECEMBER 7 NATURE NEUROSCIENCE

3 7 Nture Pulishing Group Perentge orret Perentge orret 9 9 Noise Modulted noise 7 7 Clen (nd in quiet) ws mesured. A omprison of the performne of different sites s funtion of TMR (neurometri urves) reveled tht there ould e mrked differenes in performne with the msked trgets, even for sites tht showed omprle performnes with unmsked trgets. For exmple, in one site, the disrimintion of Behvior Neurl timing Neurl rte Perentge orret d n = 9 n = Reltive trget intensity (db) Perentge orret Modulted noise d e f msked trgets ws lose to hne level (%) for low TMRs nd pprohed the unmsked performne t high TMRs (Fig. 3). In ontrst, nother site showed performne lose to hne t -db TMR, whih improved with inresing TMR, ut only up to level well elow the performne for unmsked trgets (Fig. 3). There were lso Noise Noise Modulted noise Behvior Neurl dt Figure 3 Neurl disrimintion under different msking onditions. (,) Disrimintion ury of two representtive sites, plotted s funtion of TMR (neurometri urves), in the presene of three different mskers (men ± 1 s.d.). The performne hieved with unmsked trgets (t -db level) is lso indited (tringle). Chne performne ws % (gry horizontl dshed line). () Men disrimintion in the presene of the three mskers for 9 sites (men ± s.e.m.). Two-wy repeted-mesures ANOVA showed tht there ws sttistilly signifint intertion etween TMR nd msker type (F 8,5 ¼ 17.89, P o.1), in ddition to signifint min effets of TMR (F,7 ¼ 15.81, P o.1) nd msker (F,13 ¼ 8.17, P o.1) on performne. (d) Men disrimintion of trgets in the sene of mskers for sites, when the trget intensity ws t level orresponding to eh TMR tested. Although the differenes in performne with trget intensity were found to e signifint (F,8 ¼ 17.75, P o.1, one-wy repeted mesures ANOVA), Tukey post ho omprisons showed tht this effet ws driven y the lowest intensity only, where smll, ut signifint, derese ompred with ll other intensities ws deteted (P o.1). Figure Neurl versus ehviorl performne. (,,e) Individul exmples of sites where the neurometri urve (thik solid line) mthed the men psyhometri funtion ross the ommon TMR rnge (thin solid line; gry region shows ± 1 s.d.). Also shown is the performne for the sme sites when the disrimintion ws sed on firing-rte lone (dshed lines). (,d,f) The neurometri urves for ll sites (thin lines) ompred with the men psyhometri funtion (replotted from, nd e). NATURE NEUROSCIENCE VOLUME [ NUMBER 1 [ DECEMBER 7 13

4 7 Nture Pulishing Group site-speifi differenes in performne ross the different mskers. In one instne, the performne ws est in horus, intermedite in noise nd worst in modulted noise (Fig. 3), wheres in nother, performne ws similr ross the different mskers (Fig. 3). The men neurometri performne ross 9 sites for msked trgets improved s funtion of TMR nd pprohed the men performne otined using unmsked trgets (Fig. 3). Disrimintion for unmsked trgets ross the full rnge of trget intensities (tht is, from db to + db reltive to the fixed msker intensity) ws reltively onstnt in the suset of sites in whih responses were otined(fig. 3d). Overll, the solute trget intensity did not pper to drive the disrimintion differenes tht were seen with the msked trgets. Comprison of neurl nd ehviorl performne Four zer finhes were tested ehviorlly for their ility to disriminte trget songs under identil stimulus onditions to those used in the neurl experiment (see Methods). ws similr for the three msker types, with sores lose to hne (% for the tsk used) t the lowest TMR nd with n upper symptote lose to the sore tht ws otined during trining with trgets in quiet (88%) (Fig. ). We found sites where the neurometri funtions losely mthed the psyhometri funtions ross the ommon TMR rnge (Fig.,,e). In ddition, neurl disrimintion on the sis of fine timing, rther thn men rte, provided muh etter mth to the ehviorl dt for these sites. Logisti fits to individul urves of the 9 reorded sites (see Methods) indited tht the mjority of neurometri funtions hd shllower slopes nd higher thresholds thn the psyhometri funtions (Supplementry Fig. online). Sites tht mthed the ehviorl performne over the entire rnge of TMRs tended to hve reltively high performne levels, overll nd were in the top third of the dtset if rnked on the sis of their disrimintion of unmsked trgets (Fig.,d,f). DISCUSSION Although humn nd niml listeners re remrkly dept t understnding ommunition sounds in noisy or omplex kgrounds (solving the CPP), diffiulties rise in prtiulrly dverse onditions, suh s highly reverernt environments or in the se of hering impirment. Furthermore, despite long history of reserh in rtifiil speeh reognition, no effetive omputtionl solution to the CPP is known. Investigting the neurl sustrtes for the CPP in suitle niml model my help determine the soure of the pereptul diffiulty posed y omplex listening environment nd revel how iologil systems ope with suh settings. Previous studies hve demonstrted tht songirds n detet lerned trget songs in mixtures of tsk-irrelevnt songs 1,18.Oneof these studies lso ompred the msking effets of distrting songs nd level-mthed white noise, nd found no ppreile differenes in performneetweenthetwo 18, onsistent with our findings. Notly, humn listeners often show different mounts of msking for noise nd for omplex mskers tht re spetro-temporlly similr to the trget 8,19. Although it is diffiult to mke detiled omprisons to the humn literture, our results suggest tht songirds nd humns differ in their reltive suseptiility to different msker types. This my e result of different neurl sensitivities (for exmple, spetrl nd temporl tuning), ttentionl strtegies or omintion of oth. Although the previous studies provided informtion regrding the influene of mskers on ehviorl performne of songirds, reltively little is known out the effets of mskers t the neurl level. To our knowledge, this is the first study to jointly investigte the neurl nd ehviorl disrimintion of omplex trget sounds in the presene of omplex mskers. Severl findings point to the involvement of uditory ortex in the CPP in oth humns nd nimls. Auditory ortex is importnt in the pereption of omplex sounds suh s vol ommunition sounds nd speeh,1. Physiologil studies in songirds suggest similr role for field L in proessing vol ommunition sounds 15, 7.Different sudivisions of mmmlin uditory ortex pper to hve differing responses to omplex sounds (for exmple, speeh) 1. Studies in the vin uditory forerin lso suggest distint response properties to simple versus omplex sounds 15,1,,,5, lthough detiled omprison etween the sudivisions in the mmmlin nd vin systems remins premture. Reent thinking suggests tht the uditory ortex my e ritil in uditory sene nlysis nd the formtion of uditory ojets 1,8. Although suortil proessing is undoutedly involved in the nlysis of omplex sounds 9 38, the uditory ortex is likely to mke ritil ontriution to solving the CPP. Reltively few studies hve investigted the proessing of msked trgets y ortil neurons 39. In most of those studies, the trgets used were simple stimuli suh s tones or liks, nd the trgets nd mskers were dissimilr. Given the signifint nonlinerities in ortil responses to omplex nturl sounds,7,5, it is diffiult to extrpolte the results of those studies to the CPP. Indeed, in one study, ortil responses to omplex trgets (ird hirps) in the presene of kground noise reveled mrked nonliner intertions, highlighting the importne of using omplex trgets nd mskers in the serh for ortil sustrtes of the CPP. Although we identified interferene t the ortil level, it remins possile tht some of these effets my e inherited from suortil levels of proessing. Future studies t erlier levels of the uditory system in the songird will e importnt to lrify this issue. Our results reveled two forms of interferene: the ddition of spurious spikes ourring primrily during the gps etween syllles nd the suppression of informtive spikes ourring primrily during the syllles themselves. The ddition of spikes during syllle gps is expeted to e result of the presene of msker energy. Although this effet ws oserved for ll of the mskers, the numer of dditions ws signifintly greter for modulted noise thn for rodnd noise (whih hd the sme fine struture, ut different envelope) nd horus (whih hd the sme envelope, ut different fine struture). This suggests tht oth envelope nd fine struture ontriute to the mgnitude of this form of interferene. In ontrst, the suppression of informtive spikes during the syllles ws oserved primrily for the horus nd noise mskers. Suppression might e expeted for the rodnd noise msker, s it is known tht neurl responses dpt to onstnt stimultion of this kind. However, the ft tht suppression ws seen for the horus msker nd not for the modulted noise msker indites nonliner effets due to the spetrl struture of the horus. Potentil mehnisms tht ould underlie suppression inlude ortil inhiition nd synpti depression. We found tht the different forms of ortil interferene systemtilly degrded neurl disrimintion s TMR deresed. Even sites tht disriminted very urtely without msker performed lose to hne levels t the lowest TMR ( db). In priniple, it is possile to imgine popultion oding shemes for pooling lrge popultions of neurons tht ould ompenste for the redution in performne of single sites. However, omprison of single-site performne nd ehviorl performne reveled severl unexpeted results. First, the neurometri funtions otined from some of the sites losely mthed the psyhometri funtion over the entire rnge of TMRs smpled for the neurl experiments. Although this result is reminisent of similr 1 VOLUME [ NUMBER 1 [ DECEMBER 7 NATURE NEUROSCIENCE

5 7 Nture Pulishing Group results otined in visul nd somtosensory orties,7, there is n importnt distintion. In the previous studies, neurl disrimintion ws sed on verge firing rte. In our dt, neurl performne determined y verge rte ws fr inferior to ehviorl performne, nd informtion present t finer time sles ws neessry to mth ehviorl performne. Seond, the distriution of neurometri funtions reveled tht the sites tht mthed ehviorl performne hd reltively high performne levels, rnking pproximtely in the top third of our dtset on the sis of their performne in the trgetlone ondition. Notly, we found severl ses in whih neurl performne ws higher thn ehviorl performne, t lest for ertin TMRs. Beuse the neurl nd ehviorl dt were olleted in different irds, one possile explntion of this result is vriility ross individuls; tht is, the estsites ouldhveomefromirdsthtwouldhveperformedt orrespondingly higher levels in the ehviorl tsk. Alterntive explntions for this result re sed on the downstrem redout of informtion. The neurl performne tht we oserved t the level of field L n e thought of s the informtion ville for guiding ehvior. However, the speifi mnner in whih this informtion is red out downstrem my impose further limits on performne. One possiility is tht dditionl soure(s) of noise t the redout stge ould redue neurl performne. Another possiility is tht the redout is le to ess the est neurons only fter repeted exposures vi lerning mehnism. Suh senrio suggests tht one would oserve n improvement in the psyhometri funtion over the ourse of lerning, ommon phenomenon in psyhophysil experiments. The neurl interferene reveled in this study led to profound redution in neurl disrimintion nd ws ompnied y prllel redution in ehviorl performne. This kind of interferene my lie t the hert of the diffiulty of the CPP. In rel world settings, however, there re other ftors tht my influene performne in suh tsks. First, the llotion of ttention is ruil, nd n importnt future diretion will e to exmine neurl responses nd sensitivity to interferene in wke nimls tht re pying ttention to the tsk. Seond, ehviorl studies in humns hve demonstrted tht the sptil seprtion of ompeting sound soures gretly improves listener s ility to proess soure of interest,9,17. Sptil ues n led to effetive improvements in TMR, whih might produe improvements in performne tht re preditle from the neurometri funtions mesured in this study. More importntly, however, sptil seprtion n id the seletive llotion of ttention, nd thus my intert with ttentionl mnipultions. METHODS Stimuli. Song motifs from five mle zer finhes (five renditions or tokens from eh ird) were used s trget stimuli. Stimuli were nd-pss filtered etween Hz nd 8 khz. All motifs from prtiulr ird were highly stereotypil to tht ird, ut were distint from those of other irds (see Supplementry Fig. 3 online). Three types of mskers were reted, ll with the sme long-term spetrl hrteristis, ut with different short-term sttistis. The horus mskers were generted y dding together three song motifs from nontrget irds. The noise mskers were reted y generting rodnd noise tht hd spetrl profile mthing tht of the verge of the set of horus mskers. The modulted noise mskers were generted y modulting noise msker with the envelope from rndom horus msker. Six tokens were generted for eh type of msker. Trget nd msker mixtures were reted t five different TMRs. The TMR ws defined s the rtio of the trget nd msker intensities, where intensity ws lulted using the rodnd root men squred vlue over the entire length of eh signl. Mskers were lwys presented t fixed level of 5-dB SPL (pek, A-weighted intensity mesured t 5 m from the loudspeker t the position of the irds ers), nd the TMR ws set to one of five evenly sped vlues etween db nd + db y vrying the solute intensity of the trget. For eh omintion of trget song (five), msker type (three) nd TMR (five), set of ten stimuli were generted using rndom seletions from the trget nd msker tokens. Neurl reordings. Extrellulr reordings were mde from field L of nine urethne-nesthetized, dult, mle zer finhes using tehniques desried previously 11,. The experimentl protool ws pproved y the Institutionl Animl Cre nd Use Committee, Boston University, Chrles River Cmpus. Neurl responses were mesured for unmsked trgets (presented in quiet) nd trgets emedded in the three mskers. The unmsked nd msked stimuli were rndomly interleved nd presented in the free field vi single loudspeker loted 5 m in front of the ird to otin ten trils for eh stimulus. Stimulus presenttion nd response reordings were performed vi Ntionl Instruments dt quisition ord (PCI-5E) nd ontrolled using ustom written softwre in LWindows CVI (Ntionl Instruments). For eh reording site, spike wveforms were first identified using window disrimintor with mnully set threshold, nd then further refined using prinipl omponents nlysis of the wveform shpes in Mtl (Mthworks). Of ll the sites tht were proed, the sites tht showed n verge firing rte tht ws signifintly different (P o.1, pired t-test) from the verge spontneous firing rte for t lest one song stimulus were inluded in the nlysis (n ¼ 9). The dtset ws omprised of 18 sites tht hd well-isolted spike wveforms suggesting single neuron response nd 51 sites with wveforms inditive of responses from smll lusters of two to five neurons. Here, we use the term site to refer to oth types of responses. The reording lotions were verified using Nissl-stined prsgittl -mm setions of the rin to ompre the eletrode trks to histologil mrkers tht define the oundries of field L 8. All sites were onfirmed to e in the uditory forerin on the sis of omintion of histology, stereotxi oordintes nd reording depth. Of these, out of 9 sites were from field L nd the remining nine sites were from the overlying re of the udl mesopllium, the vin nlog of seondry uditory ortex. Dt nlysis. We exmined the reorded spike trins for dditions nd deletions of spikes (reltive to the response to the trget in quiet) y mesuring firing rtes within nd etween trget song syllles. The nlysis ws done t -db TMR, s this ws the only trget level for whih unmsked responses were olleted for ll sites. For suset of sites in whih unmsked responses were olleted t trget intensities orresponding to the entire TMR rnge, the firingrte nlysis ws rried out t eh TMR. Eh trget song ws mnully segmented to mrk the syllle oundries nd the temporl gps etween syllles (Supplementry Fig. 3). The firing rtes in the unmsked nd msked onditions were lulted t eh site seprtely for the within- nd etweentrget syllle portions of the spike responses nd were verged ross trgets, trils nd syllles. The reltive differene etween the verge msked nd unmsked rte ws then omputed for eh msker. To ount for the neurl trnsmission time to field L, we nlyzed the neurl response strting ms fter the eginning of eh syllle. We evluted the ility of sites to disriminte etween trget songs using spike distne metri 9. The metri quntifies the dissimilrity etween pirs of spike trins, while permitting the time sle of the nlysis to e djusted using single free prmeter (t). For smll t, the metri ts s oinidene detetor with smll differenes in spike timing ontriuting to the distne, wheres for long t, it ts s rte-differene ounter, where verge firing rtes ontriute to the distne. Responses to unmsked trgets were ompred with the spike trins eliited y trgets emedded in the mskers using lssifition sheme sed on the spike distne metri 11,. Eh msked response ws lssified into trget song tegory y seleting the trget whose unmsked response ws losest to the oserved response. Perent orret performne in this one-in-five lssifition tsk ws omputed for eh site. For performne sed on spike timing, the temporl resolution of the distne metri ws set to ms (shown in erlier work to give optiml lssifition performne 11 ). For performne sed on spike rte, the temporl resolution ws set to 1, ms (the length of the stimulus-driven response). NATURE NEUROSCIENCE VOLUME [ NUMBER 1 [ DECEMBER 7 15

6 7 Nture Pulishing Group Sttistil testing. Differenes in men firing rtes nd disrimintion were tested using one-wy nd two-wy repeted mesures ANOVA with Sigm-Stt softwre (SysStt Softwre). When the ANOVA showed signifint min effets, pir-wise omprisons were rried out using Tukey post ho omprison proedures. We report the ANOVA results s F, ¼, where nd re the numertor nd denomintor degrees of freedom of the F sttisti. Friedmn s nonprmetri tests lso yielded similr results. Perent orret sores were rsine trnsformed efore testing. For ll tests, the null hypothesis ws rejeted t the.5 level. Behviorl experiment. The ehviorl experiment ws onduted on four zer finhes s prt of lrger experiment. All proedures were pproved y the Institutionl Animl Cre nd Use Committee, University t Bufflo. The irds were pled in ge inside sound-ttenuting smll-niml hmer lined with ousti fom. A single loudspeker loted diretly ehind the ird delivered the ousti stimuli. The irds were trined to sit on perh in the front of the ge, fing food hopper nd two miroswith response keys. Stimulus presenttion nd response reordings of the nimls were ontrolled y Sykofizx softwre nd TDT hrdwre modules (Tuker- Dvis Tehnologies). The irds were trined using opernt onditioning proedures to perform tegoriztion tsk using set of irdsong trgets tht were lmost identil to those used in the neurl study. Six trget songs were used (the five from the neurl study nd one dditionl song). The irds were trined to pek the left key to initite tril nd vrile witing intervl ( 7 s). Following tht intervl, trget song ws presented from the loudspeker. The irds were trined to pek the left key gin for three of the songs nd to pek the right key for the other three songs. The songs were rndomly ssigned to key nd eh ird hd different omintion of left nd right songs. If they responded orretly nd in s, they were rewrded with -s ess to seeds from the hopper. If they responded inorretly, house light ws extinguished for 5 s. Trining ontinued until performne rehed symptote (round 88% orret fter,, trils). Following trining, the irds were tested on the sme tegoriztion tsk in the presene of one of three oloted msker stimuli. Msker stimuli were identil to those used in the neurl study. All irds were tested t TMRs of, 1,, +1, + nd +3 db; some of the irds were lso tested t TMRs outside of this rnge ( 8, 3, +8 or + db) in some onditions, ut these dt re not presented here. Perentge orret vlues were lulted for eh ird, ollpsed ross the six trget songs, from t lest trils per TMR. Psyhometri nd neurometri funtions. Clssifition performne s funtion of TMR ws nlyzed for eh individul site nd for eh ehviorl sujet to give neurometri nd psyhometri funtions, respetively. For the extrtion of threshold nd slope prmeters, logisti funtions were fit to the rw dt using the Mtl toolox PSIGNIFIT. The lower symptote of these funtions ws fixed t the hne performne level. The upper symptote ws fixed on n individul sis t the performne level hieved for the lssifition of unmsked songs. Threshold ws defined s the TMR t the midpoint of given neurometri or psyhometri funtion. Note: Supplementry informtion is ville on the Nture Neurosiene wesite. ACKNOWLEDGMENTS This work ws supported y the US Ntionl Institute on Defness nd Other Communition Disorders grnt 1 RO1 DC 7 1A1 (K.S.), the Defness Reserh Foundtion nd the Ntionl Orgniztion for Hering Reserh Foundtion (M.D.), nd the Air Fore Offie of Sientifi Reserh grnt FA95 1 (B.S.-C.). AUTHOR CONTRIBUTIONS K.S., B.S.-C., M.D., R.N., V.B nd E.O. designed the reserh. R.N. rried out the neurophysiology experiments nd nlyzed the neurl dt. V.B. nlyzed the ehviorl dt nd ssisted in the neurophysiology experiments. E.O. generted stimuli nd ssisted in the neurophysiology experiments. E.M. nd M.D. rried out the ehviorl experiments. M.D. supervised the ehviorl experiments. K.S. supervised the neurophysiology experiments. K.S., V.B. nd R.N. wrote the mnusript. Pulished online t Reprints nd permissions informtion is ville online t reprintsndpermissions 1. Hulse, S.H., MDougll-Shkleton, S.A. & Wisniewski, A.B. Auditory sene nlysis y songirds: strem segregtion of irdsong y Europen strlings (Sturnus vulgris). J. Comp. Psyhol. 111, 3 13(1997).. Endepols, H., Feng, A.S., Gerhrdt, H.C., Shul, J. & Wlkowik, W. Roles of the uditory midrin nd thlmus in seletive phonotxis in femle gry tree frogs (Hyl versiolor). Behv. Brin Res. 15, 3 77 (3). 3. Cherry, E.C. Some experiments on the reognition of speeh, with one nd with two Ers. J. Aoust. So. Am. 5, (1953).. Bronkhorst, A.W. The oktil prty phenomenon: review of reserh on speeh intelligiility in multiple-tlker onditions. Austi 8, 9 73 (). 5. Asri, H., Perlmutter, B.A. & Zdor, A.M. Sprse representtions for the oktil prty prolem. J. Neurosi., ().. Hykin, S. & Chen, Z. The oktil prty prolem. Neurl Comput. 17, (5). 7. Bronkhorst, A.W. & Plomp, R. Effet of multiple speeh-like mskers on inurl speeh reognition in norml nd impired hering. J. Aoust. So. Am. 9, (199). 8. Brungrt, D.S., Simpson, B.D., Erison, M.A. & Sott, K.R. Informtionl nd energeti msking effets in the pereption of multiple simultneous tlkers. J. Aoust. So. Am. 1, (1). 9. Kidd, G., Jr, Mson, C.R., Rohtl, T.L. & Deliwl, P.S. Relese from msking due to sptil seprtion of soures in the identifition of nonspeeh uditory ptterns. J. Aoust. So. Am., 31 (1998).. Br-Yosef, O., Rotmn, Y. & Nelken, I. Responses of neurons in t primry uditory ortex to ird hirps: effets of temporl nd spetrl ontext. J. Neurosi., (). 11. Nryn, R., Grn, G. & Sen, K. Distint time sles in ortil disrimintion of nturl sounds in songirds. J. Neurophysiol. 9, 5 58 (). 1. Nelken, I. Proessing of omplex stimuli nd nturl senes in the uditory ortex. Curr. Opin. Neuroiol. 1, 7 (). 13. Wng, L., Nryn, R., Grn, G., Shmir, M. & Sen, K. Cortil disrimintion of omplex nturl stimuli: n single neurons mth ehvior? J. Neurosi. 7, (7). 1. Doupe, A.J. & Kuhl, P.K. Birdsong nd humn speeh: ommon themes nd mehnisms. Annu. Rev. Neurosi., (1999). 15. Gre, J.A., Amin, N., Singh, N.C. & Theunissen, F.E. Seletivity for onspeifi song in the zer finh uditory forerin. J. Neurophysiol. 89, 7 87 (3). 1. Woolley, S.M., Fremouw, T.E., Hsu, A. & Theunissen, F.E. Tuning for spetro-temporl modultions s mehnism for uditory disrimintion of nturl sounds. Nt. Neurosi. 8, (5). 17. Best, V., Ozmerl, E., Gllun, F.J., Sen, K. & Shinn-Cunninghm, B.G. Sptil unmsking of irdsong in humn listeners: energeti nd informtionl ftors. J. Aoust. So. Am. 118, (5). 18. Appeltnts, D., Gentner, T.Q., Hulse, S.H., Blthzrt, J. & Bll, G.F. The effet of uditory distrtors on song disrimintion in mle nries (Serinus nri). Behv. Proesses 9, (5). 19. Crhrt, R., Tillmn, T.W. & Greetis, E.S. Pereptul msking in multiple sound kgrounds. J. Aoust. So. Am. 5, 9 73 (199).. Fith, R.H., Miller, S. & Tlll, P. Neuroiology of speeh pereption. Annu. Rev. Neurosi., (1997). 1. Rusheker, J.P. Cortil proessing of omplex sounds. Curr. Opin. Neuroiol. 8, (1998).. Lngner, G., Bonke, D. & Sheih, H. Neuronl disrimintion of nturl nd syntheti vowels in field L of trined mynh irds. Exp. Brin Res. 3, 11 (1981). 3. Lewiki, M.S. & Arthur, B.J. Hierrhil orgniztion of uditory temporl ontext sensitivity. J. Neurosi. 1, (199).. Muller, C.M. & Leppelsk, H.J. Feture extrtion nd tonotopi orgniztion in the vin uditory forerin. Exp. Brin Res. 59, (1985). 5. Sheih, H., Lngner, G. & Bonke, D. Responsiveness of units in the uditory neostritum of the guine fowl (Numid melegris) to speies-speifi lls nd syntheti stimuli. II. Disrimintion of Imus-like lls. J. Comp. Physiol. A Neuroethol. Sens. Neurl. Behv. Physiol. 13, 57 7 (1979).. Sen, K., Theunissen, F.E. & Doupe, A.J. Feture nlysis of nturl sounds in the songird uditory forerin. J. Neurophysiol. 8, (1). 7. Theunissen, F.E., Sen, K. & Doupe, A.J. Spetrl-temporl reeptive fields of nonliner uditory neurons otined using nturl sounds. J. Neurosi., (). 8. Nelken, I., Fishh, A., Ls, L., Ulnovsky, N. & Frks, D. Primry uditory ortex of ts: feture detetion or something else? Biol. Cyern. 89, 397 (3). 9. Verhey, J.L., Pressnitzer, D. & Winter, I.M. The psyhophysis nd physiology of omodultion msking relese. Exp. Brin Res. 153, 5 17 (3).. MAlpine, D., Jing, D. & Plmer, A.R. Binurl msking level differenes in the inferior olliulus of the guine pig. J. Aoust. So. Am., 9 3 (199). 31. Jing, D., MAlpine, D. & Plmer, A.R. Responses of neurons in the inferior olliulus to inurl msking level differene stimuli mesured y rte-versus-level funtions. J. Neurophysiol. 77, 85 3 (1997). 3. Rtnm, R. & Feng, A.S. Detetion of uditory signls y frog inferior olliulr neurons in the presene of sptilly seprted noise. J. Neurophysiol., (1998). 1 VOLUME [ NUMBER 1 [ DECEMBER 7 NATURE NEUROSCIENCE

7 7 Nture Pulishing Group Plmer, A.R., Jing, D. & MAlpine, D. Desynhronizing responses to orrelted noise: mehnism for inurl msking level differenes t the inferior olliulus. J. Neurophysiol. 81, 7 73 (1999). 3. Lin, W.Y. & Feng, A.S. Free-field unmsking response hrteristis of frog uditory nerve fiers: omprison with the responses of midrin uditory neurons. J. Comp. Physiol. [A] 187, (1). 35. Pressnitzer, D., Meddis, R., Delhye, R. & Winter, I.M. Physiologil orreltes of omodultion msking relese in the mmmlin ventrl ohler nuleus. J. Neurosi. 1, (1). 3. Neuert, V., Verhey, J.L. & Winter, I.M. Responses of dorsl ohler nuleus neurons to signls in the presene of modulted mskers. J. Neurosi., (). 37. Lne, C.C. & Delgutte, B. Neurl orreltes nd mehnisms of sptil relese from msking: single-unit nd popultion responses in the inferior olliulus. J. Neurophysiol. 9, (5). 38. Rmhndrn, R., Dvis, K.A. & My, B.J. Rte representtion of tones in noise in the inferior olliulus of deererte ts. J. Asso. Res. Otolryngol. 1, 1 1 (). 39. Ls, L., Stern, E.A. & Nelken, I. Representtion of tone in flututing mskers in the sending uditory system. J. Neurosi. 5, (5).. Phillips, D.P. & Cynder, M.S. Some neurl mehnisms in the t s uditory ortex underlying sensitivity to omined tone nd wide-spetrum noise stimuli. Her. Res. 18, 87 (1985). 1. Nelken, I., Rotmn, Y. & Br Yosef, O. Responses of uditory-ortex neurons to struturl fetures of nturl sounds. Nture 397, (1999).. Furukw, S., Xu, L. & Middlerooks, J.C. Coding of sound-soure lotion y ensemles of ortil neurons. J. Neurosi., (). 3. Nieder, A. & Klump, G.M. Signl detetion in mplitude-modulted mskers. II. Proessing in the songird s uditory forerin. Eur. J. Neurosi. 13, 33 (1).. Hofer, S.B. & Klump, G.M. Within- nd ross-hnnel proessing in uditory msking: physiologil study in the songird forerin. J. Neurosi. 3, (3). 5. Mhens, C.K., Wehr, M.S. & Zdor, A.M. Linerity of ortil reeptive fields mesured with nturl sounds. J. Neurosi., 89 1 ().. Britten, K.H., Shdlen, M.N., Newsome, W.T. & Movshon, J.A. The nlysis of visul motion: omprison of neuronl nd psyhophysil performne. J. Neurosi. 1, (199). 7. Romo, R. & Slins, E. Flutter disrimintion: neurl odes, pereption, memory nd deision mking. Nt. Rev. Neurosi., 3 18 (3). 8. Fortune, E.S. & Mrgolish, D. Cytorhitetoni orgniztion nd morphology of ells of the field L omplex in mle zer finhes (Tenopygi guttt). J. Comp. Neurol. 35, 388 (199). 9. vn Rossum, M.C. A novel spike distne. Neurl Comput. 13, (1).. Mhens, C.K. et l. Single uditory neurons rpidly disriminte onspeifi ommunition signls. Nt. Neurosi., 31 3 (3). NATURE NEUROSCIENCE VOLUME [ NUMBER 1 [ DECEMBER 7 17