Cell Tissue Res (2015) 361:371–386 DOI 10.1007/s00441-015-2230-8

REVIEW

Age-related changes in sound localisation ability Claudia Freigang 1 & Nicole Richter 1,2 & Rudolf Rübsamen 1 & Alexandra A. Ludwig 1,3

Received: 2 April 2015 / Accepted: 26 May 2015 / Published online: 16 June 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Auditory spatial processing is an important ability in everyday life and allows the processing of omnidirectional information. In this review, we report and compare data from psychoacoustic and electrophysiological experiments on sound localisation accuracy and auditory spatial discrimination in infants, children, and young and older adults. The ability to process auditory spatial information changes over lifetime: the perception of the acoustic space develops from an initially imprecise representation in infants and young children to a concise representation of spatial positions in young adults and the respective performance declines again in older adults. Localisation accuracy shows a strong deterioration in older adults, presumably due to declined processing of binaural temporal and monaural spectro-temporal cues. When compared to young adults, the thresholds for spatial discrimination were strongly elevated both in young children and older adults. Despite the consistency of the measured values the underlying causes for the impaired performance might be different: (1) the effect is due to reduced cognitive processing ability and is thus task-related; (2) the effect is due to reduced information about the auditory space and caused by declined processing in auditory brain stem circuits; and (3) the auditory

* Claudia Freigang [email protected] 1

Faculty of Bioscience, Pharmacy and Psychology, University of Leipzig, Talstrasse 33, 04103 Leipzig, Germany

2

Department of Otorhinolaryngology, Head and Neck Surgery, University Medical Centre Freiburg, Elsässer Straße 2n, 79110 Freiburg, Germany

3

Department of Otorhinolaryngology, Section of Phoniatrics and Audiology, University of Leipzig, Liebigstrasse 10-14, 04103 Leipzig, Germany

space processing regime in young children is still undergoing developmental changes and the interrelation with spatial visual processing is not yet established. In conclusion, we argue that for studying auditory space processing over the life course, it is beneficial to investigate spatial discrimination ability instead of localisation accuracy because it more reliably indicates changes in the processing ability. Keywords Localisation accuracy . Minimum audible angle . Mismatch negativity . Age-related spatial processing . Hemifield code

Introduction Perception of acoustic space is an important ability in everyday life, as it aids orientation in the 3D world, enables listeners to focus their attention on a target speaker in noisy environments, and provides an immediate overview over simultaneously occurring events in the surroundings of a listener (e.g. street noises, sirens, approaching cars, etc.). The ability to localise sounds in the horizontal and vertical planes depends on the central auditory processing of binaural and monaural acoustic information. Other than in the visual or the somatosensory system, the basic spatial information is not directly encoded through a position-specific activation of the sensory epithelium. In the eye, it is the activated locus on the retina, and, in touch, the stimulated partition of the skin that establishes the basis for the central representation of spatial information. The sensory epithelium of the cochlea, the basilar membrane, just encodes spectral information. Spatial acoustic information is solely the result of neuronal processing based on the computation of monaural spectral cues that arise due to filtering characteristics of the upper body and the pinnae, and of binaural cues, i.e. differences in the time of arrival

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(interaural time differences, ITD) or differences in levels (interaural level differences, ILD) of the acoustic input at both ears (Blauert 1997). The computation of a single sound source position or of multiple sources is the capacity of signal processing within neuronal circuitries formed within and across the nuclei of the ascending auditory pathway from the brain stem up to the auditory cortex. It has long been known that auditory space processing changes with age, which suggests that central processing of auditory information undergoes significant developmental changes. To get a better understanding of these changes, this review summarises our current knowledge on two aspects of spatial acoustic perception, (1) sound localisation and (2) spatial discrimination, based upon studies performed in children, as well as in young and older adults. To present the facts in a concise way, the review will only deal with the performance in the horizontal plane. Measuring auditory space processing Auditory space processing can be assessed by measuring localisation performance in the acoustic free-field or lateralisation performance under headphone conditions. The latter has the advantage that both binaural cues ITD and ILD can be manipulated independently, allowing for a better understanding of the underlying physiological mechanisms. Also, there are low demands on the experimental setup and the acoustic conditions under which the measurements are performed, which makes it an ideal setting to be used in rehabilitation facilities and clinics. What might be regarded as a disadvantage is that the earphone stimulation creates a rather arbitrary auditory perception (unless individual head-related transfer functions, HRTFs, are used for signal presentation), which hampers the testing of more complex or natural spatial acoustic stimulus conditions. The alternative approach is to use free-field stimulus conditions in anechoic chambers, since it enables the presentation of acoustic stimuli in a 3D space under controlled seminatural conditions. Auditory space processing has often been assessed by two different types of psychoacoustic measures: absolute localisation accuracy and spatial discrimination performance, the latter an indication of auditory spatial resolution (Mills 1958; Perrott and Saberi 1990). Localisation accuracy tasks quantify how accurately a sound source can be localised. This is mostly achieved by using a pointing task, where participants are instructed to indicate the perceived position of a sound source (Shankweiler 1961; Seeber et al. 2010; Kerber and Seeber 2012; Kühnle et al. 2012; Schmiedchen et al. 2012, 2013; Freigang et al. 2014a) or by alignment of the participant’s head and gaze to the direction of the sound source (Lewald et al. 2000). Another paradigm used to measure the localisation accuracy is the absolute identification task (Abel et al. 2000), where participants have to indicate the sound direction by choosing one of several indicated sound source positions in an n-

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alternative forced-choice task. Sound localisation is quantified in terms of absolute error, signed error and precision (Hartmann 1983). The absolute error is calculated as the rootmean square error (RMSE) between the target position and the pointed position. The signed error (SE) is calculated as the difference between the target and the response position and indicates the direction of the pointing error, e.g. in azimuthal testing, did participants point towards more medial or more lateral positions. Further, localisation performance can be quantified in terms of the consistency of the responses, i.e. as the amount of variance across trials. It is also useful to calculate regression models with correlation coefficients based on the relationship between the response angle and the target angle. Lastly, regression analyses are often used to analyse localisation accuracy in terms of the bias (error) and the gain. Auditory spatial discrimination is mostly studied by using the minimum audible angle (MAA) paradigm introduced by Mills (1958). The MAA is defined as the smallest distance between two neighbouring sound sources that can be discriminated, and the MAA thus represents a threshold for auditory spatial acuity—an indicator of auditory spatial resolution. The MAA paradigm was initially applied in tests using a twoalternative forced-choice (2AFC) procedure, where participants had to indicate whether the probe tone was presented to the left or the right of the standard tone. Responding to criticisms that pointed out that these tests measure absolute identification performance rather than the actual spatial discrimination ability (Hartmann and Rakerd 1989), recent studies have made use of the three-alternative forced-choice (3AFC) procedure (Freigang et al. 2014a, b; Kühnle et al. 2012; Briley and Summerfield 2014).

Localisation and spatial discrimination of sounds, and neuronal representation of the acoustic space Young adult listeners When presenting simple sounds such as pure tones, ITDs are the most dominant cue for azimuthal localisation at low frequencies 2.5 kHz. This phenomenon is referred to as Rayleigh’s duplex theory (Blauert 1997). The basis for ILD processing is the acoustic shadow cast by the head to the ear positioned away from the sound source. The processing of ITDs crucially depends on the precise encoding of the temporal fine structure (TFS) of sound waves both with respect to frequency and amplitude profiles. The encoding of TFS information is provided by the unique ability of neurons in secondand third-order nuclei of the auditory brain stem to synchronise their action potentials to a particular phase of the basilar membrane vibration—a mechanism referred to as phase locking. When using more complex sounds, such as

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amplitude-modulated pure tones at high frequencies, it has been demonstrated that listeners are also sensitive to the ITD of sound envelopes (McFadden and Pasanen 1976). For localisation of broadband sounds, human listeners most dominantly use the ITD cue of the TFS (Stevens and Newman 1936; Wightman and Kistler 1992). In healthy young humans, auditory localisation accuracy for static stimuli is best for broadband sounds presented at the centre of the median plane with a localisation error ranging between 2° and 3.5°, and declines towards lateral positions to an error of about 10° (Makous and Middlebrooks 1990). Though not a major concern, it needs to be mentioned that monaural cues, specifically the spectrotemporal content of acoustic signals, also play an important role in auditory localisation, namely for resolving front–back confusions and for vertical localisation (Middlebrooks and Green 1991; Makous and Middlebrooks 1990). For many years, the ability to discriminate spatially distinct acoustic sources was acquired by quantifying the MAA. Mills (1958) who introduced the MAA paradigm reported best discrimination at central positions with thresholds of about 1°–2°; at lateral positons, spatial discrimination declined and MAA thresholds increase to about 10°. When focussing on the (pre-attentive) processing of sound source information at cortical levels, electroencephalography (EEG) has often been used under free-field stimulus conditions (Paavilainen et al. 1989; Röder et al. 1996, 1999, 2001; Teder-Sälejärvi and Hillyard 1998; Deouell et al. 2006, 2007; Röttger et al. 2007; Richter et al. 2009, 2013; Bennemann et al. 2013; Briley et al. 2013). These experiments provided evidence for the ‘opponent-channel coding’ hypothesis, the basis of which were in vivo electrophysiological experiments on laboratory animals (Phillips and Irvine 1981; McAlpine and Grothe 2003; Werner-Reiss and Groh 2008). Further described under the name of ‘hemifield model’ the concept was also proposed for the representation of sound direction in humans (Stecker and Middlebrooks 2003; Magezi and Krumbholz 2010; Salminen et al. 2009, 2010, 2012; Briley et al. 2013; review Phillips 2008). The model proposes two neural populations in each cortical hemisphere showing graded sensitivity to acoustic stimulation in the contralateral hemifield. When considering the entire neuron population, the activation level should be maximal for lateral stimulus positions and gradually decline towards central positions. One particular feature of the model is that central positions can be represented with high spatial resolution, while lateral positions are less accurately represented. Neural adaptation paradigms probing the neural change response at the level of auditory cortex is one of two frequently used magnetoencephalographic (MEG)/EEG-paradigms to study the underpinning neural encoding of auditory space (Salminen et al. 2012). In this paradigm, an adaptor sound is presented from a standard position immediately followed by a probe sound from a different spatial position and the change

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response—in the N1-P2 time window corresponding to the probe sound—is quantified. Salminen et al. (2009, 2010) reported that in MEG change responses to adaptors in the same hemifield were smaller than when the probe and adaptor sounds were presented in opposite hemifields. Magezi and Krumbholz (2010) investigated the opponent channel code for ITDs in humans under headphone conditions and found that change responses to probe sounds were largest when an inward change occurred, i.e. when the ITD changed from 500 to 0 μs, as opposed to an outward change. Briley et al. (2013) examined auditory cortical responses to adaptor-probe stimuli across a broad range of azimuthal positions and found supporting evidence for the hemifield code. Additionally, they reported inter-hemispheric differences for sound position: the left hemisphere revealed larger responses for contralateral stimuli, suggesting a contralateral dominance. However, responses in the right auditory cortex were similar for probes in both hemifields. Woldorff et al. (1999) investigated the contribution of each cortical hemisphere to the processing of lateralised stimuli in MEG and functional magnet resonance imaging (fMRI) to monaural and binaural FM-sweep tone bursts (lateralised with an ITD of 2 ms). For monaural stimuli, a strong contralateral activation was found in fMRI and MEG. However, the binaural sounds did not evoke lateralised brain activity, but instead a symmetric activation in both hemispheres. The authors interpreted their results in the light of the binaural neural inputs (i.e. contralateral and ipsilateral projections from the brain stem) to auditory cortex neurons sensitive to ITD (excitatory from both ears, ∼35 % of neurons) or ILD (contralateral excitatory, ipsilateral inhibitory, ∼65 % of neurons) inputs (for review, see Clarey et al. 1992). They concluded that, in cases of monaural stimulation, where the ILD was maximal, the contralateral dominance is based on the large number of contralaterally excited ILD neurons. For the binaural stimuli, a contralateral activation was also predicted. The lack of such an effect was thought to be a result of the unphysiological ITD of 2 ms, i.e. cortical neurons were not sensitive to such large ITDs and hence a contralateral dominance was absent. When considering both, the fact that central representation of auditory space almost entirely depends on the neuronal processing ability in the central auditory system and the finding of age-related changes in central nervous processing (Canlon et al. 2010, see BDevelopmental and age-related changes in the auditory system^), it has to be expected that auditory localisation and/or discrimination will change throughout the life span. Infants, children, and adolescents There are only a few studies devoted to spatial hearing in infants (localisation accuracy: Muir and Field 1979; Muir et al. 1979, review 1989; Muir and Clifton 1985; for review,

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see Muir and Hains 2004; Morrongiello and Rocca 1987; MAA: Ashmead et al. 1987; Morrongiello 1988; Morrongiello et al. 1990) and young children (localisation accuracy: Van Deun et al. 2009; Grieco-Calub and Litovsky 2010; Lovett et al. 2012; Kühnle et al. 2012; Otte et al. 2013; MAA: Morrongiello 1988; Litovsky 1997; Lovett et al. 2012; Kühnle et al. 2012). Localisation accuracy in infants has been measured by quantifying the head turning towards an off-midline sound source. Muir and Field (1979) showed that head turning to rattle sounds presented at 90° to the left and right of the midline is reliable (80 % correct responses) in new-born infants. According to Muir et al. (1979, review see 1989), localisation accuracy follows a U-shaped function from the first to the fourth month after birth, i.e. first localisation accuracy is relatively accurate and declines in the third and fifth month and reaches a more stable representation in 7-month-old infants. These changes have been associated with developmental factors related to a suppression of subcortical mechanisms and also to a switch to cortical mechanisms in infants aged about 1 month (Muir and Clifton 1985; Muir and Hains 2004). Slugocki and Trainor (2014) investigated the dip in the localisation response by measuring MMN and the mismatch response1 in infants aged 2, 5, 8, and 13 months, and their results revealed that even in 2-month-old infants the cortex receives spatial information. Thus, based on their findings, the authors concluded that the reason for the absence of a proper localisation response might be an inability to use the spatial auditory information in order to generate an appropriate motor response. Also, the extent of head movement was quantified, revealing that new-borns turned their head further to the side for sound sources at 90° than at 45°, i.e. the head motion was selective. Muir and Clifton (1985) found that 4.5month-old-infants were able to turn their head towards sounds displaced by 30°. Morrongiello and Rocca (1987) measured the localisation accuracy in a larger setup with 10 loudspeakers in the horizontal plane in infants aged 6–18 months. They found a mean localisation error of 16.9° for central and para-lateral positions and smaller errors for lateral sounds. It should be noted that measuring head movements in infants is problematic, as it is not clear whether the alignment of the head is identical to the perception of the sound source. It is possible that eye movements are also involved, and the respective contributions of head and eye movements were not differentiated. Also, it is not clear whether motor development poses another constraint on this method. It seems more appropriate to measure MAA in infants when aiming at a quantification of spatial acuity. Using this

approach, Ashmead et al. (1987) investigated MAA by measuring discrimination to left- and rightward-displaced sounds in infants aged between 26 to 30 weeks. The MAAs were in the range of about 19°, which is considerably larger than MAAs in young adults (ranging about 1°–2°). Morrongiello (1988) tested the MAA in infants, and young children 6, 9, 12, 15, and 18 months of age at central positions using white noise stimuli and found that spatial resolution increased from about 12° in the youngest age group to 4° in 18-month-old children. In a later study, Morrongiello et al. (1990) investigated MAA thresholds in 8- to 24-week-old infants in an observer-based setting, since head movements become less frequent at that age and thus constitute a less reliable measure. The authors found an increase in localisation acuity with age similar to their previous study from 27° in 8week-old infants to 18° in 24-week-old infants. Litovsky (1997) used the precedence effect2 to investigate the MAA in young children aged 18 months, in children aged 5 years, and in young adults (19–21 years). Noise bands (0.5– 8.0 kHz), 25 ms in duration, were presented at midline positions and at various angular deviations to the left and to the right. The MAA threshold was assessed by presenting the sounds in a single interval and by using a 1-up/2-down procedure. For the young children, detection of spatial changes of stimulus locations was inferred from an immediate reaction of the child to the change. Five-year-old children and young adults were instructed to point to the direction of change in the location, whenever they perceived a shift away from the midline. MAA thresholds were 6° in 18-month-old children, 2° in 5-year-old children and 1° in young adults. The group of 5-year-olds were characterised by large variance, i.e. the threshold of some children was close to that measured for the young children, while the performance in others was almost like in young adults. It was concluded that 5-yearolds potentially might be in a transitional stage with some children having gained the ability to discriminate like young adults, while others lag behind. However, the authors did not exclude the possibility that different attentional capacities in children might be the cause of variance in the data of this age group. Van Deun et al. (2009) compared the localisation accuracy in children aged 4–6 years and in adults (19–29 years) in the frontal acoustic space between −60° to the left and +60° to the right using a bell-like broadband signal. Participants from both age groups indicated the position of the sound source by pointing towards the perceived speaker in a 9-AFC task. No significant difference in mean localisation accuracy was reported between 5-year-old children and adults (RMSE was about 6°), but localisation errors were significantly increased

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2

The mismatch response has been described by Trainor et al. (2003) as a slow positive wave between 100 and 500 ms after stimulus onset in infants.

The precedence effect refers to the phenomenon of echo suppression in sound source localisation (for review, see Litovsky et al. 1999).

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in the 4-year-olds. The authors concluded that the binaural hearing capacities in 5-year-olds are comparable to those in adults. The differences found between the 4-year-old children and adults was thought to be attributable to the development in binaural hearing lagging behind and to cognitive factors such as attention, task comprehension, and testing conditions. In another study, localisation accuracy and acuity was measured in 5-year-old children to the speech sound Bbaseball^ by using the absolute identification procedure involving 7 or 15 speakers (i.e., 7- and 15-AFC) ranging from 70° to the left to 70° to the right in the frontal field (Grieco-Calub and Litovsky 2010; see also Litovsky 2011). The respective RMSEs were between 8.9° and 29.2° with a mean RMSE of 18.3°, which exceed the values reported by Van Deun et al. (2009). The difference may be associated with differences in the acoustic stimulus and the experimental protocol. Possibly, the 15-AFC task imposed a higher task demand which increased the level of difficulty for these children. Lovett et al. (2012) investigated localisation accuracy and spatial discrimination for speech stimuli in children aged between 1.5 and 7.9 years and in young adults (20–24 years). Localisation accuracy was measured as percentage correct in an absolute identification task using speech sounds presented at 60°, 30°, and 15° to the left and to the right. The performance improved across the age span tested, and adult levels of performance were reached in children aged 6 years. Additionally, the study explored the spatial discrimination abilities at frontal positions using a left–right discrimination paradigm. The spatial differences tested were 30° or 60° to the left or to the right of the frontal reference position. A 100 % percent correct result was measured in young adults and in children aged 3 years. The authors attributed the failure of younger children (

Age-related changes in sound localisation ability.

Auditory spatial processing is an important ability in everyday life and allows the processing of omnidirectional information. In this review, we repo...
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