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Cortical network differences in the sighted versus early blind for recognition of human-produced action sounds

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Cortical network differences in the sighted versus early blind for recognition of human-produced action sounds
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  r  H uman  B rain  M apping 32:2241–2255 (2011)  r Cortical Network Differences in the Sighted VersusEarly Blind for Recognition of Human-ProducedAction Sounds  James W. Lewis, 1,2 *  Chris Frum, 1,2  Julie A. Brefczynski-Lewis, 1,2,3 William J. Talkington, 1,2 Nathan A. Walker, 1,2 Kristina M. Rapuano, 1,2 and Amanda L. Kovach 1,2 1 Department of Physiology and Pharmacology, West Virginia University, Morgantown, West Virginia 2 Center for Advanced Imaging, West Virginia University, Morgantown, West Virginia 3 Department of Radiology, West Virginia University, Morgantown, West Virginia r r Abstract:  Both sighted and blind individuals can readily interpret meaning behind everyday real-worldsounds. In sighted listeners, we previously reported that regions along the bilateral posterior superiortemporal sulci (pSTS) and middle temporal gyri (pMTG) are preferentially activated when presentedwith recognizable action sounds. These regions have generally been hypothesized to represent primaryloci for complex motion processing, including visual biological motion processing and audio–visual inte-gration. However, it remained unclear whether, or to what degree, life-long visual experience mightimpact functions related to hearing perception or memory of sound-source actions. Using functionalmagnetic resonance imaging (fMRI), we compared brain regions activated in congenitally blind versussighted listeners in response to hearing a wide range of recognizable human-produced action sounds(excluding vocalizations) versus unrecognized, backward-played versions of those sounds. Here, weshow that recognized human action sounds commonly evoked activity in both groups along most of theleft pSTS/pMTG complex, though with relatively greater activity in the right pSTS/pMTG by the blindgroup. These results indicate that portions of the postero-lateral temporal cortices contain domain-spe-cific hubs for biological and/or complex motion processing independent of sensory-modality experience.Contrasting the two groups, the sighted listeners preferentially activated bilateral parietal plus medialand lateral frontal networks, whereas the blind listeners preferentially activated left anterior insula plus bilateral anterior calcarine and medial occipital regions, including what would otherwise have been vis-ual-related cortex. These global-level network differences suggest that blind and sighted listeners maypreferentially use different memory retrieval strategies when hearing and attempting to recognize actionsounds.  Hum Brain Mapp 32:2241–2255, 2011 .  V C  2011  W iley  P eriodicals,  I nc. Keywords:  hearing perception; episodic memory; mirror-neuron systems; cortical plasticity; fMRI r r Contract grant sponsor: NCRR NIH COBRE; Contract grantnumber: E15524.*Correspondence to: James W. Lewis, Center for Advanced Imag-ing, and Department of Physiology and Pharmacology, PO Box9229, West Virginia University, Morgantown, WV 26506-9229.E-mail: jlewis@hsc.wvu.eduReceived for publication 23 December 2009; Revised 27 August2010; Accepted 7 September 2010DOI: 10.1002/hbm.21185Published online 8 February 2011 in Wiley Online Library(wileyonlinelibrary.com). V C  2011  W iley  P eriodicals,  I nc.  INTRODUCTION Is the human cortical organization for sound recognitioninfluenced by life-long visual experience? In young adultsighted participants, we previously identified left-lateral-ized networks of ‘‘high-level’’ cortical regions, well beyondearly and intermediate processing stages of auditory cortexproper, which were preferentially activated when every-day, nonverbal real-world sounds were judged as accu-rately recognized—in contrast to hearing backward-playedversions of those same sounds that were unrecognized[Lewis et al., 2004]. These networks appeared to include atleast two multisensory-related systems. One systeminvolved left inferior parietal cortex, which was latershown to have a role in audio-motor associations thatdepended on handedness [Lewis et al., 2005, 2006] and tooverlap mirror-neuron systems in both sighted [Rizzolattiand Craighero, 2004; Rizzolatti et al., 1996] and blind lis-teners [Ricciardi et al., 2009]. Another system involved theleft and right postero-lateral temporal regions, whichseemed consistent with functions related to audio–visualmotion integration or associations. This included the pos-terior superior temporal sulci (pSTS) and posterior middletemporal gyri (pMTG), herein referred to as the pSTS/pMTG complexes.Visual response properties of the pSTS/pMTG com-plexes have been well studied. The postero-lateral tempo-ral regions are prominently activated when viewingvideos of human (conspecific) biological motions [Johans-son, 1973], such as human face or limb actions [Beau-champ et al., 2002; Calvert and Brammer, 1999; Calvertand Campbell, 2003; Grossman and Blake, 2002; Grossmanet al., 2000; Kable et al., 2005; Puce and Perrett, 2003; Puceet al., 1998] and point light displays of human actions [Saf-ford et al., 2010]. In congenitally deaf individuals, cortexoverlapping or near the pSTS/pMTG regions show agreater expanse of activation to visual motion processingwhen monitoring peripheral locations of motion flowfields [Bavelier et al., 2000], attesting to a prominent rolein visual motion processing.Hearing perception studies have also revealed a promi-nent role of the pSTS/pMTG complexes in response tohuman action sounds (i.e., conspecific action sounds,excluding vocalizations), which may be regarded as one dis-tinct category of action sound. This includes, for example,assessing footstep movements [Bidet-Caulet et al., 2005], dis-criminating hand-tool action sounds from animal vocaliza-tions [Lewis et al., 2005, 2006], and hearing hand-executedaction sounds relative to environmental sounds [Gazzolaet al., 2006; Ricciardi et al., 2009]. Furthermore, the pSTS/pMTG complexes show category-preferential activation forhuman-produced action sounds when contrasted withaction sounds produced by nonhuman animals or nonlivingsound-sources such as automated machinery and the natu-ral environment [Engel et al., 2009; Lewis et al., in press].The pSTS/pMTG regions, anatomically situated midway between early auditory and early visual processing corti-ces, are also commonly implicated in functions related toaudio–visual integration, showing enhanced activations toaudio–visual inputs derived from natural scenes, such astalking faces, lip reading, or observing hand tools in use[Beauchamp et al., 2004a,b; Calvert et al., 1999, 2000;Kreifelts et al., 2007; Olson et al., 2002; Robins et al., 2009;Stevenson and James, 2009; Taylor et al., 2006, 2009]. Suchfindings have provided strong support for the proposalthat the postero-lateral temporal regions are primary locifor complex natural motion processing [for reviews seeLewis, 2010; Martin, 2007]. Postscanning interviews fromour earlier study [Lewis et al., 2004] revealed that some of the sighted participants would ‘‘visualize’’ the sound-source upon hearing it (e.g., visualizing a person’s handstyping on a keyboard). One possibility was that visualassociations or ‘‘visual imagery’’ might have been evoked by the action sounds when attempting to recognize them,thereby explaining the activation of the bilateral pSTS/pMTG complexes. Thus, one hypothesis we sought to testwas that if the pSTS/pMTG regions are involved in someform of visual imagery of sound-source actions, then thereshould be no activation of these regions in listeners whohave never had visual experience (i.e., congenitally blind).In addition to probing the functions of the pSTS/pMTGcomplexes, we additionally sought to identify differencesin global network activations (including occipital cortices)that might be differentially recruited by congenitally blindlisteners. A recent study using hand-executed actionsounds reported activation to more familiar sounds nearmiddle temporal regions in both sighted and blind listen-ers [Ricciardi et al., 2009]. However, their study focusedon fronto-parietal networks associated with mirror-neuronsystems or their analogues in blind listeners. Thus, itremained unclear what  global  network differences mightexist between sighted and blind listeners for representingacoustic knowledge and other processes that are related toattaining a sense of recognition of real-world sounds.Congenitally blind listeners are reported to show bettermemory for environmental sounds after physical orsemantic encoding [Roder and Rosler, 2003]. Numerousstudies involving early blind individuals indicate that occi-pital cortices, in what would otherwise have been predom-inantly visual-related cortices, become recruited tosubserve a variety of other functions and possibly confercompensatory changes in sensory and cognitive process-ing. For instance, occipital cortices of blind individuals areknown to adapt to facilitate linguistic functions [Burton,2003; Burton and McLaren, 2006; Burton et al., 2002a,b;Hamilton and Pascual-Leone, 1998; Hamilton et al., 2000;Sadato et al., 1996, 2002], verbal working memory skills[Amedi et al., 2003; Roder et al., 2002], tactile object recog-nition [Pietrini et al., 2004], object shape processing[Amedi et al., 2007], sound localization [Gougoux et al.,2005], and motion processing of artificial (tonal) acousticsignals [Poirier et al., 2006]. Thus, a second hypothesis wesought to test was that the life-long audio–visual-motorexperiences of sighted listeners, relative to the audio-motor r  L ewis et al.  rr  2242  r  experiences of blind listeners, will lead to large-scale net-work differences in cortical organization for representingknowledge, or memory, of real-world human actionsounds. MATERIALS AND METHODSParticipants Native English speakers with self reported normal hear-ing and who were neurologically normal (excepting visualfunction) participated in the imaging study. Ten congeni-tally blind volunteer participants were included (averageage of 54; ranging from 38 to 64, seven female, one left-handed), together with 14 age-matched sighted control(SC) participants (average age 54; ranging 37 to 63, sevenfemale; one left-handed). We obtained a neurologic historyfor each blind participant using a standard questionnaire.The cause of blindness for nine participants was retinopa-thy of prematurity (formerly known as retrolental fibropla-sia), and one participant had an unknown cause of  blindness. All reported that they had lost sight (were toldthey had lost sight) at or within a few months after birth,and herein referred to as early blind (EB). Some partici-pants reported that they could remember seeing shadowsat early ages ( < 6 years) but could never discriminate vis-ual objects. All EB participants were proficient Braillereaders. We assessed handedness with a modified Edin- burgh handedness inventory [Oldfield, 1971], based on 12questions, substituting for blind individuals the question‘‘preferred hand for writing’’ with ‘‘preferred hand forBraille reading when required to use one hand.’’ Informedconsent was obtained for all participants following guide-lines approved by the West Virginia University Institu-tional Review Board, and all were paid an hourly stipend. Sound Stimuli and Delivery Sound stimuli included 105 real-world sounds describedin our earlier study [Lewis et al., 2004], which were com-piled from professional CD collections (Sound Ideas, Rich-mond Hill, Ontario, Canada) and from various web sites(44.1 kHz, 16-bit, monophonic). The sounds were trimmedto   2 s duration (1.1–2.5 s range) and were temporallyreversed to create ‘‘backward’’ renditions of those sounds(Cool Edit Pro, Syntrillium Software, now owned byAdobe). The backward-played sounds were chosen as acontrol condition because they were typically judged to beunrecognizable, yet were precisely matched for many low-level acoustic signal features, including overall intensity,duration, spectral content, spectral variation, and acousticcomplexity. However, the backward sounds did necessar-ily differ in their temporal envelopes, having differentattacks and offsets. Sound stimuli were delivered using aWindows PC computer, using Presentation software (ver-sion 11.1, Neurobehavioral Systems) via a sound mixerand MR compatible electrostatic ear buds (STAX SRS-005Earspeaker system; Stax, Gardena, CA), worn under soundattenuating ear muffs. Stimulus loudness was set to a com-fortable level for each participant, typically 80–83 dBC-weighted in each ear (Bru¨el & Kjær 2239a sound meter),as assessed at the time of scanning.During each fMRI scan, subjects indicated by three alter-native forced choice (3AFC) right hand button presswhether they (1) could recognize or identify the sound(i.e., verbalize, describe, imagine, or have a high degree of certainty about what the likely sound-source was), (2)were unsure, or (3) knew that they did not recognize thesound. Each participant underwent a brief training session just before scanning wherein several backward- and for-ward-played practice sounds were presented: If the partic-ipant could verbally identify it then they were affirmed of this and instructed to press button no. 1. If he or she hadno idea what the sound-source was or could only hazarda guess, then they were instructed to press button no. 3.Participant’s were instructed that they could use a second button press (button no. 2) for instances where they werehesitant about identifying the sound or felt that if givenmore time or a second presentation that they might beable to guess what it was. Each backward-played soundstimulus was presented before the corresponding forward-played version within a scanning run to avoid potentialpriming effects; participants were not informed that the‘‘modified’’ sounds were simply played backwards. Over-all, this paradigm relied on the novelty of having partici-pants hearing each unique sound out of context for thefirst time, and their indication of whether or not the soundevoked a sense of a recognizable action event. The sightedindividuals were asked to keep their eyes closed through-out all of the functional scans. Magnetic Resonance Imaging and Data Analyses Scanning was conducted on a 3 Tesla General ElectricHorizon HD MRI scanner using a quadrature bird-cagehead coil. For the main paradigm, we acquired whole-head, spiral in and out imaging of blood-oxygenated leveldependent (BOLD) signals [Glover and Law, 2001], usinga clustered-acquisition fMRI design which allowed soundstimuli to be presented during scanner silence [Edmisteret al., 1999; Hall et al., 1999]. A sound or a silent eventwas presented every 9.3 s, with each event being triggered by the MRI scanner. Button responses and reaction timesrelative to sound onset were collected during scanning.BOLD signals were collected 6.5 s after sound or silentevent onset (28 axial brain slices, 1.875    1.875    4.00mm 3 spatial resolution, TE  ¼  36 ms, OPTR  ¼  2.3 s volumeacquisition, FOV  ¼  24 mm). This volume covered theentire brain for all subjects. Whole brain T1-weighted ana-tomical MR images were collected using a spoiled GRASSpulse sequence (SPGR, 1.2 mm slices with 0.9375    0.9375mm 2 in plane resolution). r  H uman  A ction  S ound  R ecognition in the  B lind  rr  2243  r  Data were viewed and analyzed using AFNI and relatedplug-in software-http://afni.nimh.nih.gov/ [Cox, 1996].Brain volumes were motion corrected for global headtranslations and rotations by registering them to the 20th brain volume of the functional scan closest to the anatomi-cal scan. BOLD signals were converted to percent signalchanges on a voxel-by-voxel basis relative to responses tothe silent events within each scan. For each participant,the functional scans (seven separate runs) were concaten-ated into a single time series. We then performed multiplelinear regression analyses based on the button responsesmodeling whole-brain BOLD signal responses to the soundstimuli relative to the baseline silent events. With the clus-tered acquisition design, the BOLD response to each soundstimulus could be treated as an independent event. In par-ticular, brain responses to stimulus events could be cen-sored from the model in accordance with eachparticipant’s button responses. Because participants wereinstructed to listen to the entire sound sample andrespond as accurately as possible (3AFC) as to their senseof recognition, rather than as fast as possible, an analysisof reaction times was not reliable. For the main analysis of each individual dataset, we included only those soundpairs where the forward-played version was judged to berecognizable (RF, Recognized Forward; button no. 1) andthe corresponding backward-played version was judged asnot being recognizable (NB, Not recognized Backward; button no. 3).For this study, several sound stimulus events were addi-tionally censored  post hoc  from all analyses for all individ-uals. This included censoring nine of the sound stimulithat contained vocalization content, which were excludedto avoid confounding network activation associated withpathways that may be specialized for processing vocaliza-tions [Belin et al., 2004; Lewis et al., 2009]. Additionally,we subsequently excluded sounds that were not directlyassociated with a human agent instigating the action. Toassess human agency, five age-matched sighted partici-pants not included in the fMRI scanning rated all soundson a Likert scale (1–5) indicating whether the heard sound(without reference to any verbal or written descriptions)evoked the sense that a human was directly involved inthe sound production (1  ¼  human, 3  ¼  not sure, 5  ¼  notassociated with human action). Sounds with an averagerating between 1 and 2.5 were analyzed separately ashuman-produced action sounds, resulting in retaining 61of the 108 sound stimuli (Appendix).Using AFNI, individual anatomical and functional brainmaps were transformed into the standardized Talairachcoordinate space [Talairach and Tournoux, 1988]. Func-tional data (multiple regression coefficients) were spatiallylow-pass filtered (6-mm box filter), then merged by com- bining coefficient values for each interpolated voxel acrossall subjects. A voxel-wise two sample  t -test was performedusing the RF versus NB regression coefficients to identifyregions showing significant differences between the EBand SC groups. The results from this comparison were re-stricted to reveal only those regions showing positive dif-ferences in RF versus NB comparisons (i.e., where RFsounds led to greater positive BOLD signal changes in atleast one of the two groups of listeners). This approachexcluded regions differentially activated solely due to dif-ferential negative BOLD signals, wherein the unrecognized backward-played sounds evoked greater magnitude of activation relative to recognized sounds for both groups.Corrections for multiple comparisons were based on aMonte Carlo simulation approach implemented by AFNI-related programs AlphaSim and 3dFWHM. A combinationof individual voxel probability threshold ( t -test,  P  <  0.02or  P  <  0.05; see Results) and the cluster size threshold (12or 20 voxel minimum, respectively), based on an estimated2.8 mm 3 full-width half-max spatial blurring (before low-pass spatial filtering) present within individual datasets,yielded the equivalent of a whole-brain corrected signifi-cance level of   a  <  0.05.Data were then projected onto the PALS atlas braindatabase using Caret software-http://brainmap.wustl.edu[Van Essen, 2005; Van Essen et al., 2001]. Surface-regis-tered visual area boundaries—e.g., V1 and V2 [Hadjikhaniet al., 1998]—from the PALS database were superimposedonto the cortical surface models, as were the reportedcoordinate and approximated volumetric locations of theleft and right parahippocampal place area (PPA) [Epsteinand Kanwisher, 1998; Gron et al., 2000]. Portions of thesedata can be viewed at http://sumsdb.wustl.edu/sums/directory.do?id  ¼  6694031&dir_name  ¼  LEWIS_HBM10,which is part of a database of surface-related data fromother brain mapping studies. RESULTS To reveal brain regions preferentially involved in the pro-cess of recognizing the human-produced action sounds, foreach individual, we effectively subtracted the activationresponse to the unrecognized, backward-played soundsfrom that for the corresponding recognized, forward-playedhuman action sounds (refer to Methods). There was no sta-tistical difference in the distribution of numbers of retainedsound pairs between the two groups (see Appendix inset;30.6% for EB, 35.9% for SC; two sample, two-tailed  t -test, T  (22) ¼ 1.48;  P > 0.15), indicating that the EB and SC groupswere comparable overall in their ability to recognize theparticular everyday sound stimuli retained for analyses.The resulting group-averaged patterns of cortical activationto recognized forward-played sounds relative to unrecog-nized backward-played sounds are illustrated on the PALScortical surface model for the SC group (Fig. 1A, yellow vs.dark green,  t -test;  T  (14)  ¼  2.65,  P  <  0.02, 12 voxel minimumcluster size correcting to  a  <  0.05) and the EB group (Fig.1B, red vs. blue;  T  (10)  ¼  2.82,  P  <  0.02,  a  <  0.05). Although both the forward- and backward-played sounds stronglyactivated cortex throughout most of auditory cortexproper—including primary auditory cortices residing along r  L ewis et al.  rr  2244  r  Figure 1. Comparison of cortical networks for sighted versus early blindlisteners associated with recognition of human action sounds.All results are illustrated on 3D renderings of the PALS corticalsurface model, and all colored foci are statistically significant at a  <  0.05, whole brain corrected.  A : Group-averaged activationresults from age-matched sighted participants ( n  ¼  14) whenhearing and recognizing forward-played human action sounds(RF, yellow) in contrast to not recognized backward-played ver-sions of those sounds (NB, green).  B : Group-averaged activationin the early blind ( n  ¼  10) for recognized, forward-played (RF,red) versus unrecognized backward-played (RB, blue) soundstimuli.  C : Regions showing direct overlap with the same(orange) or opposite (green) differential activation pattern. Allhistograms illustrate responses to recognized forward-played(RF) sounds and the corresponding backward-played sounds notrecognized (NB) relative to silent events for both groups. Out-lines of visual areas (V1, V2, V3, hMT, etc., white outlines) arefrom the PALS atlas database. CaS, calcarine sulcus; CeS, centralsulcus; CoS, collateral sulcus; IFG, inferior frontal gyrus; IPS,intraparietal sulcus; STS, superior temporal sulcus. The IFGfocus did not directly intersect the cortical surface model, andthus an approximate location is indicated by dotted outline.Refer to color inset for color codes, and the text for otherdetails. [Color figure can be viewed in the online issue, which isavailable at wileyonlinelibrary.com.] r  H uman  A ction  S ound  R ecognition in the  B lind  rr  2245  r
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