www.elsevier.com/locate/cogbrainres

Cognitive Brain Research

Research report

Distinct fMRI responses to laughter, speech, and sounds along the

human peri-sylvian cortex

Martin Meyera,b,T, Stefan Zyssetb, D. Yves von Cramonb, Kai Alterb,c

aDepartment of Neuropsychology, University of Zurich, Treichlerstrasse 10, CH-8032 Zurich, SwitzerlandbMax Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany

cSchool of Neurology, Neurobiology, and Psychiatry, Newcastle Auditory Group, University of Newcastle, UK

Accepted 7 February 2005

Available online 29 March 2005

Abstract

In this event-related fMRI study, 12 right-handed volunteers heard human laughter, sentential speech, and nonvocal sounds in which

global temporal and harmonic information were varied whilst they were performing a simple auditory target detection. This study aimed to

delineate distinct peri-auditory regions which preferentially respond to laughter, speech, and nonvocal sounds. Results show that all three

types of stimuli evoked blood–oxygen-level-dependent responses along the left and right peri-sylvian cortex. However, we observed

differences in regional strength and lateralization in that (i) hearing human laughter preferentially involves auditory and somatosensory fields

primarily in the right hemisphere, (ii) hearing spoken sentences activates left anterior and posterior lateral temporal regions, (iii) hearing

nonvocal sounds recruits bilateral areas in the medial portion of Heschl’s gyrus and at the medial wall of the posterior Sylvian Fissure

(planum parietale and parietal operculum). Generally, the data imply a differential regional sensitivity of peri-sylvian areas to different

auditory stimuli with the left hemisphere responding more strongly to speech and with the right hemisphere being more amenable to

nonspeech stimuli. Interestingly, passive perception of human laughter activates brain regions which control motor (larynx) functions. This

observation may speak to the issue of a dense intertwining of expressive and receptive mechanisms in the auditory domain. Furthermore, the

present study provides evidence for a functional role of inferior parietal areas in auditory processing. Finally, a post hoc conjunction analysis

meant to reveal the neural substrates of human vocal timbre demonstrates a particular preference of left and right lateral parts of the superior

temporal lobes for stimuli which are made up of human voices relative to nonvocal sounds.

D 2005 Elsevier B.V. All rights reserved.

Theme: Neural basis of behavior

Topic: Cognition

Keywords: Speech; Laughter; Vocal timbre; Functional Magnetic Resonance Imaging (fMRI); Peri-sylvian region; Auditory cortex

1 Notably, Heschl’s gyrus in its entirety does not exclusively accom-

modate primary auditory cortex [77]. Cytoarchitectonic and morphometric

1. Introduction

Converging evidence obtained from a plethora of clinical

and neuroimaging observations points to a residence of

speech and auditory bottom-up functions in the superior

temporal lobes of both cerebral hemispheres [5–7,11,12,23,

39,41,45,46,50,52–55,60,68,73,85,86,101,107,112]. Con-

0926-6410/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.cogbrainres.2005.02.008

T Corresponding author. Department of Neuropsychology, University of

Zurich, Treichlerstrasse 10, CH-8032 Zurich, Switzerland. Fax: +41 44 634

4342.

E-mail address: mmeyer@access.unizh.ch (M. Meyer).

sistently, these studies demonstrate a sequence of sensory

and cognitive processes mediated by brain regions stretching

along from the primary auditory cortex (PAC)1 into different

24 (2005) 291–306

studies rather demonstrate that the primary auditory cortex (PAC) usually

covers the most medially situated two thirds of Heschl’s gyrus [67].

However, human auditory areas are not confined to the PAC but are

presumed to extend across the surface of the supratemporal plane (STP),

including the planum polare (PPol) and the planum temporale (PT) even

into the insula (INS) and the parietal operculum (PaOp) [78].

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306292

anterior and posterior parts of the peri-sylvian cortex and

superior temporal sulcus (STS), either on the left or right

hemisphere, depending on the acoustic or linguistic com-

plexity of stimuli. Numerous recent neuroimaging studies

compared speech and nonspeech stimuli (e.g., white noise

bursts, sine wave tones, frequency-modulated tones, ampli-

tude-modulated tones) to distinguish between brain regions

that are more sensitive to speech and nonspeech stimuli

[11,73,87]. However, by comparing spoken language with

nonspeech auditory cues, one has to consider a multitude of

aspects in which speech and nonvocal sounds may differ, for

example, vocal timbre. Therefore, the present study uses

human laughing as experimental condition. In terms of

phonetics, human laughter is akin to speech as it also

consists of syllable-like units but it provides less F0-

variation, monotonous articulatory movements, and a differ-

ent rhythmical structure. Perception of both speech and

laughter therefore requires rapid temporal processing but the

latter to a lesser degree. This makes laughter an interesting

acoustic stimulus to examine, since the perception of

laughter may activate the same brain regions as speech to

a certain extent but can also be considered a holistic

percept which may convey relevant paralinguistic and

affective information in the context of communication. In

this context, the brain’s right hemisphere enters the

limelight as recent neuroimaging research has brought

up some unspecific evidence which associates the right

hemisphere with paralinguistic processes during speech

perception [53,62]. The specific role the right hemisphere

may play during processing vocal sounds has been

vaguely indicated [6,7,56]. In particular, the studies

conducted by Belin et al. uncovered an enhanced

sensitivity to paralinguistic vocal information of the right

superior temporal sulcus and gyrus while the contralateral

structures appear to be more amenable to linguistic

information during spoken language comprehension

[7,26]. These findings are not in agreement with recent

studies which propose a functional segregation of the

temporal lobes with extending activity from posterior

anterior sites as a function of increasing acoustic com-

plexity. More specifically, these studies place posteriome-

dial portions of the superior temporal lobe as preQ

ferentially supporting the analysis of the complex acoustic

structure of sounds. Secondly, they identify anteriolateral

regions such as lateral STG and planum polare (PPol) to

be preferentially activated by linguistically relevant

information available in speech sounds [10,45,82,

84,85,87,88]. Here, we present data obtained from an

event-related fMRI study which sought to reconcile these

competing claims. Akin to recent studies [7,87], we

examined brain responses to connected speech and non-

vocal sounds to distinguish linguistic and auditory

processing. However, this study is novel in that we

contrasted speech and nonvocal sounds to human laughter

in order to learn more about the functional segregation of

human cortical auditory system.

1.1. What makes laughter so special?

Little is known about brain mechanisms of laughter.

Generally, laughter can be considered a vocal expressive

communicative signal and was there before man developed

speech [79]. A recent review article suggested that expres-

sive laughter can be associated with an demotionally drivenTsystem involving the amygdala, thalamic/hypo-, and

subthalamic areas and with a dvoluntaryT system originat-

ing in the premotor/frontal opercular area and leading

through the motor cortex [105]. Clinical studies observed

patients suffering from neurological disorders which

caused dpathological laughterT that is inappropriate,

mood-independent, and uncontrollable laughter. However,

it seems that pathological laughter originates from numer-

ous pathological factors during brain disease rather from

emerging from circumscribed lesions to particular brain

sites [72]. Apparently, expressive laughter may be a

phenomenon so complex that it cannot be assigned to

any single brain area but depends on the temporal

coordination of several areas constituting a functional

network. This view receives partial support by recent brain

imaging data which report a network incorporating left

insula, bilateral amygdala and bilateral auditory cortices

subserving the perception of human laughter [80]. Notably,

activity in the right auditory cortices was stronger than in

contralateral areas of the left hemisphere. According to the

authors, this rightward asymmetry of supratemporal activ-

ity may be explained in terms of a right auditory cortex

specialization for processing changes of pitch, timbre, and

tonal patterns. While these authors used silence and human

crying as baseline conditions in their study, we contrast

human laughing with speech and nonvocal sounds to

reveal a potential functional sensitivity of peri-sylvian

regions.

In terms of phonetics, laughter and speech have

essential acoustic underpinnings in common. First, speech

and laughter share the same source of vocalization [75].

Like speech, laughter can also be described as a stream of

acoustic cues which unfold in time. Typically, laugh

bursts form a phrase-like sequence of repetitive laugh

pulses that are initiated by an ingression (see Methods

section). Laughter involves the respiratory system and the

vocal apparatus and is produced by changes in the vocal and

sub-glottal, respiratory tracts as well as in the musculoske-

letal system [19] that result in staccato-like syllabic vocal-

izations. Like speech, a sequence of laughter syllables can

be combined into utterances. These utterances start with a

vocalized inhalation and consist of a series of short laugh

pulses with almost constant time intervals [66,76]. The

reiteration of syllables with their specific segmental

characteristics enables us to identify it as laughter. In

contrast to speech, laughter contains less F0-variance.

Laughter has a rich harmonic structure [74] and spectral

qualities like formant frequencies can be evaluated [3].

Interestingly, both speech and laughter arise from laryngeal

2 Example sound files are available at dhttp://www.psychologie.unizh.ch/neuropsy/home_mmeyer/BRES-D-04-06566T.

3 http://www.praat.org.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 293

modulations, modified to some degree by supralaryngeal

activity, but in terms of laughter only to a small extent

by articulation. Laughter also contains effects of one

type of co-articulation at syllable-level between the

aspiration onset and the following vowel (/h-a/), but it

is more invariant than speech as vowel quality does not

alter within laughing sequences. Differences between the

two types of vocalization can be observed with regard to

the organization of syllables contained in speech and

laughing utterances. The isochronous reiteration of

syllables in laughter is untypical for normal speech. To

summarize, hearing speech requires the processing of

rapid changes in frequency which reflect co-articulatory

information between single segments, syllable, and word

boundaries, while perceiving laughter involves the

processing of rhythmical aspects and stereotyped changes

in the fundamental frequency as melodic variation is

more prominent in each laugh burst than in each speech

syllable [79]. Notably, slow processing of prosodic and

melodic modulations has been tied to right temporal lobe

functions [56,63,64]. Here, we hypothesize that hearing

human laughter is likely to preferentially drive right

auditory fields as hearing laughter has formerly been

observed to activate the right auditory cortex more

strongly than contralateral areas [80]. Furthermore, when

volunteers hear laughter, we may expect to find activity

in the right anterior STS area as this region has been

associated with nonspeech vocal sounds [6,7,26,99].

In summary, this study aimed to explore the hemody-

namic responses within the peri-sylvian cortex to three

different classes of auditory stimuli (human laughter,

speech, and nonvocal sounds) while participants per-

formed an auditory target detection task. The event-

related design applied with the present study allowed us

to investigate transient brain responses to single exper-

imental stimuli without any confound by differential

attentional levels as we used an auditory target detection

which required the participants only to respond to

specific target trials which did not enter the data

analysis. In other words, volunteers were not explicitly

required to indicate and classify speech, laughter, and

nonvocal sounds, but to simply listen to the inflowing

stimuli which was meant to factor out potential task

effects.

In agreement with expertise provided so far, we

hypothesize that hearing sentences activates anteriolateral

regions of the peri-sylvian cortex with the left hemi-

sphere playing a prominent role as the left STG and the

left IFG have been attributed to auditory sentence

processing [21,22,31,61,63–65]. By regarding laughter

and nonvocal sounds, we expect to find stronger

bilateral or even rightward responses in the human

auditory cortex since several recent studies pointed to a

specialization of a right auditory cortical swathe for

aspects of auditory processing outside the speech

domain [42,89,104,110,114].

2. Materials and methods

2.1. Participants

12 neurologically healthy right-handed volunteers par-

ticipated in this study (mean age 24 years old; range 20 to

32 years old; 6 females and 6 males). We obtained written

consent from all participants. All volunteers were native

speakers of German and had no hearing problem.

2.2. Stimuli and design

This study comprises 3 conditions and one target

condition2:

! Speech: short sentences containing a subject noun phrase

and an intransitive verb such as dPeter sleepsT;! Sounds: nonvocal sounds;! Laughter: 10 female and 10 male laughing phrases;

! Target condition: reiterated sequence of non-sense

syllables (dlalalaT).

2.3. Acoustic analyses

One representative sound file of each condition was

subjected to acoustic analyses to demonstrate differential

temporal and harmonic characteristics. The Praat software3

was used to do acoustic analyses of auditory events.

The wave form in Fig. 1A demonstrates that speech

incorporates a continuous stream of syllables. Like speech,

laughter also shows a syllable-like reiterated sequence of

laugh bursts with an initial aspiration followed by a vowel

/a/ and decreasing amplitude envelope as a function of

time (Fig. 1B). Human vocal sounds such as speech and

laughter contain more variation in the time signal due to

typical speech characteristics such as co-articulation

between single segments, syllable, and word boundaries

and a decreasing amplitude envelope. The sound signal

(Fig. 1C), however, shows less variance in the time and

amplitude structures. On the other hand, both sounds and

laughter show an equivalent distance between laugh bursts

representing the temporal structure which differs from that

for spoken languages.

Fig. 2 shows the wide band spectrograms (0–3 kHz) of

speech (Fig. 2A), laughter (Fig. 2B), and sounds (Fig. 2C).

The figure illustrates the resonance characteristics of the

human vocal tract, that is, frequency bands with higher

amplitude in periodic parts of the signals for speech and

laughter. These frequency bands – the formants – are typical

for human vocal production. These formants transitions

reflect articulatory movements in the vocal tract which are

more variable in speech than in laughter. In other words,

Fig. 2. Wide band spectrogram of acoustic stimuli. This figure shows the

wide band spectrogram (analysis width (s) = 0.005) generated from one

speech event (A), one laughing cycle (B), and one sound event (C).

Frequency changes in both the formant and harmonic structure are typical

for vocal events (speech and laughter) and reflect articulatory dynamics in

the vocal tract. See text for details.

Fig. 1. Wave forms of acoustic stimuli. This figure shows time wave forms

for (A) one speech event (dLotte pfbelt.T), (B) one laughing cycle, and (C)

one sound event. Distances between auditory events reveal the rhythmical

structure and normalized amplitude shows balanced intensity of auditory

stimuli. See text for details.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306294

rapid changes in frequency reflect effects of co-articulation

typical for speech and to a lesser extent for laughter. In

contrast to human vocal sounds like speech and laughter, a

less dynamic frequency spectrum can be observed for

nonvocal sounds. Furthermore, sounds are composed of

single frequency components without the typical speech like

frequency and time variation.

To summarize, the acoustic observations of the material

used in this study, the time wave form (Fig. 1) reflects

temporal characteristics and differences between human

vocal sounds and nonvocal sounds. In speech and

laughter, segments and syllables are connected via co-

articulation. Boundaries of syllables and even words can

be detected. In nonvocal sounds, only the repetitive

character of a re-iterant sound event is observable. The

resonance characteristics, that is, the filtering properties of

the resonance body of the human vocal tract for speech

and laughter (Figs. 2A and B) reflect the presence of (at

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 295

least the first three) formants in the vocalic parts of human

sounds like speech and laughter and their dynamic

transitions, that is, rapid changes in frequency due to

articulatory movements of the tongue, the jaw, and other

articulators. Nonvocal sounds comprise simply superim-

posed and connected single frequencies and lack speech

like dynamic frequency variations (Fig. 2C). The source

characteristics also differ between the signals. By compar-

ing human speech, laughter, and nonvocal sounds, it

becomes obvious that the harmonic structure of the latter

is less dynamic than in human vocal sounds. However, due

to a different temporal organization of laughter consisting of

repeated single laugh syllables, the harmonic dynamics in

laughter is reduced to syllabic nuclei, that is, to the vowel

/a/, whereas in speech, it is distributed over all voiced parts

and thus displays more variance. Furthermore, nonvocal

sounds are not produced by periodic vibrations of vocal

cords in the larynx and show higher frequencies for the first

harmonics. Taken together, the acoustic analysis demon-

strates the presence of vocal cues in human laughter and

spoken sentences and the absence of vocal cues in the

sounds we used.

Auditory stimulation did not differ in level, location, nor

movement of vocal and nonvocal sounds. Speech files

were recorded from a trained female speaker. The laughing

samples were provided by a regional Radio and TV station

(Mitteldeutscher Rundfunk). The sounds were taken from a

freely distributed sound data base (Macintosh). All

conditions were equalized in length (1.5–2.3 s) and

normalized for amplitude. The four conditions were

digitized at a 16 bit/16 kHz sampling rate and presented

in a random order. The relation between image acquisition

and trial presentation was systematically varied so that

numerous time points along the response are sampled [16]

yielding an doversamplingT with a de facto sampling rate

of 2.5 Hz and an average interstimulus-interval of 8 s. In

each functional run, each condition was repeated 15 times

and during the first and last 16 s of each run no trials were

presented, giving a total duration of 10 min and 32 s per

run. In total, participants underwent 5 runs, even though

some participants were only presented with 4 runs for

technical reasons.

2.4. Procedure

Participants were comfortably placed supine in the

scanner and heard stimuli in pseudo-randomized order to

enable event-related data analysis. Cushions were used to

reduce head motion. The sounds were presented diotically

through specially constructed, MR compatible headphones

(Commander XG, Resonance Technology, Northridge,

USA). A combination of sound proof headphones and

perforated ear plugs which conducted the sound directly

into the auditory passage were used to attenuate the

scanner noise without reducing the quality of speech

stimulation.

2.5. Task

It has been shown that actively calling a subject’s

attention toward an auditory stimulus yields increased

activation in auditory fields [51,111]. To avoid a confound

between stimulus perception and attentional demands, we

utilized a simple target detection task.

2.6. MR Imaging

MRI data were collected at 3 T using a Bruker 30/100

Medspec system (Bruker Medizintechnik GmbH, Ettlingen,

Germany). The standard bird cage head coil was used.

Before MRI data acquisition, field homogeneity was

adjusted by means of dglobal shimmingT for each subject.

Then, scout spin echo sagittal scans were collected to define

the anterior and posterior commissures on a midline sagittal

section. For each subject, structural and functional (echo-

planar) images were obtained from 12 axial slices (6 mm

thickness, 2 mm spacing, 64 � 64 with a FOVof 19.2 mm)

parallel to the plane intersecting the anterior and posterior

commissures (AC–PC plane). The six inferior slices were

positioned below the AC–PC plane and the remaining six

slices extended dorsally. The whole range of slices covered

all parts of the peri-sylvian cortex and extended dorsally to

the supplementary motor area (SMA). After defining the

slices’ position, a set of two-dimensional T1 weighted

anatomical images (MDEFT sequence: TE = 20 ms, TR =

3750 ms, in-plane resolution 0.325 mm2) were collected in

plane with the echo-planar images to align the functional

images to the 3D-images [71,94]. A gradient-echo EPI

sequence was used with a TE 30 ms, angle 908, TR = 2000

ms. In a separate session, high-resolution whole-head 3D

MDEFT brain scans (128 sagittal slices, 1.5 mm thickness,

FOV 25.0 � 25.0 � 19.2 cm, data matrix of 256 � 256

voxels) were acquired additionally for reasons of improved

localization.

2.7. Data analysis

Data were analyzed with LIPSIA software [58]. During

reconstruction of the functional data, the 5 (resp. 4)

corresponding runs were concatenated into a single run.

Data preparation proceeded as follows: slice-wise motion

correction (time step 20 as reference), sinc interpolation in

time (to correct for fMRI slice acquisition sequence);

baseline correction (cut-off frequency of 1/80 Hz). To align

the functional data slices onto a 3D stereotactic coordinate

reference system, a rigid linear registration with six degrees

of freedom (3 rotational, 3 translational) was performed.

The rotational and translational parameters were acquired on

the basis of the 2-dimensional MDEFT and EPI-T1 slices to

achieve an optimal match between these slices and the

individual 3D reference data set. The resulting parameters,

scaled to standard size, were then used to transform the

functional slices using trilinear interpolation, so that the

Table 1

Laughter vs. Speech: in this table and in Table 2, results of direct comparison of laughter vs. speech and sounds are listed

Location BA Left hemisphere Right hemisphere

Z score Cluster size x y z Z score Cluster size x y z

Laughter N Speech

PrCG 6 – – – – – 3.36 463 28 �16 47

PrCG 6 – – – – – 3.63a – 49 5 23

HG/ROp/subCG 41 – – – – – 3.89 2701 47 �13 12

PT 40 – – – – – 3.57 734 55 �37 24

STP/HG/subCG 22 3.60 1218 �47 �25 12 – – – – –

Speech N Laughter

IFG (triangularis)/

post IFS

9/45 �3.48 773 �43 17 27 – – – – –

FOp (triangularis) 45/44 �3.98 1688 �40 20 6 – – – – –

STG/STS 22/42/21 �4.86 11,714 �59 �13 6 �3.73 450 49 �22 3

Post MTG 39 �3.31a – �47 �63 11 – – – – –

Z scores indicate the mean activation in a particular anatomical structure. Localization of coordinates correspond to the location of local maximal activation and

is based on standard Talairach brain space. Distances are relative to the intercommissural (AC–PC) line in the horizontal (x), anterior–posterior ( y), and vertical

(z) directions. Functional activation was thresholded at jZ z 3.09j (uncorrected alpha-level 0.001). The table only lists activation clusters exceeding a minimal

size of 225 mm3 (5 measured voxels).a Indicates that Z score refers to local maximum as this cluster is not distinct but overlaps with the cluster listed in the line above. Stereotactic coordinates are

assigned to anatomical locations by using the dAutomatic anatomical labelingT tool [92] as implemented in the MRICRO software packages (http://

www.psychology.nottingham.ac.uk/staff/cr1/mricro.html). Anatomical labels are abbreviated as follows: IFG = inferior frontal gyrus, IFS = inferior frontal

sulcus, PrCG = precentral gyrus, subCG = subcentral gyrus, PaOp = parietal operculum, HG = Heschl’s gyrus, FOp = Frontal operculum, ROp = Rolandic

operculum, PT = planum temporale, PPar = planum parietale, STG = superior temporal gyrus, STS = superior temporal sulcus, MTG = middle temporal gyrus,

FG = fusiform gyrus, IOG = inferior occipital gyrus.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306296

resulting functional slices were aligned with the stereotactic

coordinate system. This linear normalization process was

improved by a subsequent processing step that performs an

additional non-linear normalization [91].

Statistical evaluation was based on a least-square

estimation using the general linear model for serially auto

correlated observations [2,14,32,109]. First, for each

subject, statistical parametric maps were generated. The

design matrix was generated with the standard hemody-

namic response function, its first and second derivative

and a response delay of 6 s. The model equation,

including the observation data, the design matrix, and

the error term, was convolved with a Gaussian kernel of

dispersion of 4 sec FWHM. Thereafter, contrast maps (i.e.,

estimates of the raw-score differences of the beta

coefficients between specified conditions) were generated

Table 2

Laughter vs. Sounds: functional activation indicated separately for direct contrast

Location BA Left hemisphere

Z score Cluster size x y

Laughter N Sounds

HG/STG 41/42/22 – – –

Fund STS 6 – – –

FG 19 – – –

Sounds N Laughter

HG/Ppar/PaOp 22/40/41 �8.34 12,438 �44 �STG/Ppar/PaOp 22/40 – – –

Post. MTG 39 �4.82a – �44 �IFG (orbitalis) 47/10 �3.46 308 �28

For explanations, see Table 1.

for each subject and the differences between conditions

were calculated using the t statistic. Subsequently, t values

were transformed into Z scores. As the individual func-

tional data sets were all aligned to the same stereotactic

reference space, a group analysis was subsequently

performed. Group activations were calculated by the

Gaussian test at corresponding voxels [14]. To protect

against false positive activations, only regions with Z score

greater than 3.1 (P b 0.001; uncorrected) and with a

volume greater than 225 mm3 (5 measured voxels) were

considered [15,27] (Tables 1 and 2).

We also computed an additional post hoc conjunction

analysis to reveal the neural substrates of vocal timbre. For

this purpose, we determined the significant clusters which

demonstrated common activation in both the laughter vs.

sounds and the speech vs. sounds contrast (Table 3).

s between Laughter and Sounds

Right hemisphere

z Z score Cluster size x y z

– – 3.60 884 52 �16 9

– – 3.58 381 40 �37 12

– – 3.62 1491 37 �58 �6

34 24 – – – –

– – �4.42 8173 37 �34 27

60 �14 – – – – –

32 �3 – – – – –

Table 3

Conjunction analysis [Laughter vs. Sounds \ Speech vs. Sounds]: clusters indicate regions which conjunctively activate during vocal timbre (speech and

laughter vs. sounds)

Location BA Left hemisphere Right hemisphere

Z score Cluster size x y z Z score Cluster size x y z

Laughter vs. Sounds \ Speech vs. Sounds

Medial HG 41 – – – – – – 459 40 �33 9

Anterior STG 22 – 54 �56 �6 9 – 594 58 �3 6

IOG 19 – 378 �44 �72 �3 – – – – –

FG 37 – 135 �35 �78 �9 – 999 28 �51 �9

For explanations, see Table 1.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 297

Furthermore, we performed a post hoc dregion of interestT(ROI) analysis which enabled us to compute condition-

specific event-related time courses to uncover differential

involvement of particular cortical sites. We collected BOLD

signals from six bilateral ROIs along the peri-sylvian cortex.

We selected these regions since they have been demon-

strated to mediate cardinal speech and auditory functions,

namely anterior superior temporal gyrus (LH aSTG: �58,

�12, 1; RH aSTG 55, �11, 2) [11,30,45,82,84,85,88],

medial part of Heschl’s gyrus (LH mdHG: �43, �18, 9; RH

mdHG: 40, �12, 5) [42,80], posterior STG (LH pSTG:

�48, �40, 15; RH pSTG: 49, �34, 14) [38,42,55,69,108],

planum parietale (LH Ppar: �54, �30, 25; RH Ppar: 56,

�32, 26) [33,40,49,55,60], parietal operculum (LH PaOp:

�40, �28, 23; RH PaOp: 40, �28, 26) [33,40,49,55,73,

78,90,108], and subcentral gyrus (LH subCG: �49, �10,

12; RH subCG: 48, �11, 12) [79].4 The signal was collected

from the voxel with the highest regional activation in the

average Zmap originating from separate contrasts for each

single condition (laughter, speech, sounds) when compared

to empty trials. The signal was averaged time-locked to the

onset of each stimulus presentation and across all 12

subjects.

3. Results

Fig. 3 displays the main fMRI results, the contrasts

between Laughter vs. Speech, Laughter vs. Sounds, and the

conjunction analysis Vocal timbre vs. Sounds5.

3.1. Laughter vs. speech

Fig. 3A illustrates that several right peri-sylvian areas

more strongly subserved laughter when compared to speech,

namely the PT, HG/ROp, the subCG, and the ventrolateral

precentral gyrus/sulcus (PrCG). Note that the medial strip of

4 An additional Figure showing the position of ROIs projected on brain

macroanatomy is available online (dhttp://www.psychologie.unizh.ch/neuropsy/home_mmeyer/BRES-D-04-06566T).5 Due to spatial restrictions we are not comprehensively discussing the

Speech vs. Sounds contrast here. Brain scans, Tables, and results

originating from the contrast Speech vs. Sounds are available at dhttp://www.psychologie.unizh.ch/neuropsy/home_mmeyer/BRES-D-04-06566T.

the supratemporal plane (STP) in the left hemisphere also

shows stronger activity for laughter relative to speech.

Hearing normal speech relative to laughter revealed

considerable activity in the left peri-sylvian cortex along

the superior temporal gyrus (lateral convexity) extending

into the STS, STP, and in the pars triangularis of the frontal

operculum (FOp). Furthermore, extra-sylvian activity was

observed in the left posterior MTG. Stronger right hemi-

sphere responses to speech relative to laughter were found

in the middle part of the right STG/STS.

3.2. Laughter vs. sounds

As apparent from Fig. 3B, stronger hemodynamic

responses to laughter as compared to sounds were collected

from right hemisphere sites, namely from the HG/STG,

from the fund of the STS, and from the FG. Hearing sounds

relative to laughter involves medial parts of the left and right

Heschl’s gyrus (HG), the Ppar, the PT, the posterior insula,

and the PaOp bilaterally. Furthermore, we observed

activation in the left posterior MTG and in the left pars

orbitalis of the IFG at the border to the anterior insula/

posterior orbital gyrus6.

3.3. Vocal timbre vs. nonvocal sounds

The post hoc conjunction analysis to identify regions

which commonly activate during both speech and laughter

processing revealed bilateral temporal and occipital sites

with the right hemisphere demonstrating stronger involve-

ment. As apparent from Fig. 3C and Table 3, hearing vocal

sounds (speech and laughter) relative to nonvocal sounds

more strongly activates bilateral sections of the anterior

lateral STG. The right medial part of HG lining the posterior

insula also shows starker engagement. Furthermore, hearing

vocal timbre activated the left inferior occipital gyrus (IOG)

as well as both the left and right fusiform gyrus (FG). Taken

together, based on consideration of clusters’ size, we

observed a considerable functional rightward asymmetry

during perception of vocal timbre.

6 The latter cluster is depicted on a supplementary Figure available at

(dhttp://www.psychologie.unizh.ch/neuropsy/home_mmeyer/BRES-D-04-

06566T).

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306298

3.4. ROI analyses

Data obtained from six bilateral ROIs for each of the

three conditions evinces different local maxima in distinct

regions of the peri-sylvian cortex (Figs. 4–6).

Speech comprehension evoked the most considerable

responses in the left temporal cortex, in particular in lateral

parts of the anterior and posterior STG when compared to

sounds and laughter. Left hemisphere dominance for speech

was observed for temporal ROIs (aSTG, pSTG). A general

rightward asymmetry of hemodynamic responses to laughter

was found in four out of six ROIs (aSTG, pSTG, Ppar,

subCG). The strongest responses to laughter relative to

speech and sounds were collected from bilateral subCG with

a salient peak in the right subCG. Notably, time courses for

laughter overlapped with time courses for speech in eight

out of twelve ROIs in both the left (mdHG, Ppar, PaOp,

subCG) and the right hemisphere (aSTG, pSTG, Ppar,

PaOp).

For sound processing, we consistently observed stronger

RH activity in all ROIs (except mdHG). Compared to speech

and laughter, hemodynamic responses to sounds were

strongest in five out of six temporo-parietal ROIs (LH +

RH Ppar, LH + RH PaOp, LH subCG), but only in two out of

six supratemporal ROIs (LH + RH mdHG).

Summing up the major results, the data provide clear

evidence that the three different conditions preferentially

activated distinct areas. Hearing speech primarily involved

areas in the lateral convexity of the left superior temporal

region with the anterior and posterior STG obviously

playing a prominent role. Hearing laughter preferentially

recruited right hemisphere areas. Interestingly, areas in the

transition zone between parietal auditory fields and motor

cortex turned out to be considerably activated by laughter.

Hearing sounds most strongly activated bilateral regions

along the medial convexity of the posterior supratemQ poral

plane (HG, PT, Ppar) up to the parietal operculum with the

right hemisphere consistently producing stronger responses.

4. Discussion

This event-related fMRI study reveals distinct regions in

the human auditory cortex during auditory perception of

speech, vocal non-speech (laughter), and nonvocal sounds

and indicates a functional division of peri-sylvian structures.

Previous brain imaging studies have already been discussing

a functional segregation of temporal regions during auditory

processing but ignored consideration of vocal non-speech

stimuli [9,11] or confounded vocal and non-vocal sounds

Fig. 3. (A) Functional inter-subject activation for the contrast Laughter vs.

Speech. The brain scans show direct comparison between laughter (hot

colors) and speech (cold colors) on left (up x = �54, down x = �47), right

(up x = 51, down x = 49) parasagittal and horizontal (z = 8) sections (jZ z3.09j, uncorrected alpha-level 0.001). In this figure and in b and c,

functional inter-subject activation (N = 12) is superimposed onto a

normalized white-matter segmented 3D reference brain. Thus, the brain’s

white matter is separated from grey matter so that the cortical layers (the

outermost 3 to 5 mm) are removed. (B) Functional inter-subject activation

for the contrast Laughter vs. Nonvocal sounds. The brain scans show direct

comparison between laughter (hot colors) and sounds (cold colors) on left

(up x = �54, down x = �40), right (up x = 55, down x = 43) parasagittal

and horizontal (z = 8) sections (jZ z 3.09j, uncorrected alpha-level 0.001).

(C) Conjunction analysis [Laughter vs. Sounds \ Speech vs. Sounds]. The

brain scans show cluster which commonly activated during perception of

speech and laughter relative to nonvocal sounds. Overlapping responses to

human vocal timbre are depicted on two horizontal (up z = 9, down z = 6)

and two right parasagittal (up x = 43, down z = 38) sections.

Fig. 4. Averaged percent signal change collected from six bilateral regions of interest. The signal was collected from the voxel with the highest activation in the

average Z map voxels. The signal was averaged time-locked to the onset of each stimulus presentation and across all 12 subjects. aSTG = anterior superior

temporal gyrus, mdHG = medial Heschl’s gyrus, pSTG = posterior superior temporal gyrus, Ppar = planum parietale, PaOp = parietal operculum, subCG =

subcentral gyrus.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 299

which made it difficult to properly distinguish between peri-

sylvian regions subserving speech and nonspeech percep-

tion. In order to address this issue more carefully, we

presented three different types of auditory stimuli, namely

sentential vocal speech, human laughter, and nonvocal

sounds. All three types of auditory percepts evoked brain

responses in the peri-sylvian cortex bilaterally with the level

and spatial distribution of activation varying as a function of

experimental condition.

The implications of our findings for auditory processing

in distinct portions of the peri-sylvian cortex are discussed

in turn.

4.1. Speech

Our data on perception of sentential speech are mostly

confirmatory with published work in the field [29,47,84],

so we refrain from elaborating on what has been

comprehensively described elsewhere. In brief, our con-

trasts clearly show that perception of intelligible sentential

speech particularly involves brain regions along the entire

lateral STG and STS, and in the left lateral FOP. In

general, this pattern of consistent brain activation is in

agreement with a host of neuroimaging studies which

observed bilateral recruitment of superior temporal areas

while volunteers heard intelligible sentential speech

[20,22,31,62,70,82,85].

More precisely, comprehending speech signals necessi-

tates the decoding of information from differing linguistic

domains, for example, meaning of words, thematic, and

structural relations, as well as from simple sound-based

signals comprised of multiple co-occurring frequencies

called formants. Recent brain imaging studies identified

distinct brain regions, especially in left peri-sylvian cortex

subserving particular aspects of linguistic and non-linguistic

aspects of speech comprehension [10,11,28,30,31,45]. In

Fig. 5. Time course of mean event-related hemodynamic responses collected from three bilateral regions of interest in the superior temporal lobe.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306300

other words, speech comprehension can be considered a

hierarchical series of processing stages to translate sounds

into meaning [22]. Both simple sound-based and abstract

higher-level aspects of speech comprehension recruit

cortical areas on the undulating surface of the STP as well

as the insula and the deep frontal operculum [12,36,64] as

well as areas stretching along the lateral convexity of the

STG down to the temporal poles. Our ROI analyses

uncovered two regions in the left superior temporal gyrus

which have formerly been identified as subserving speech

comprehension. Due to the present understanding, the

posterior superior temporal gyrus supports the processing

of rapidly changing acoustic cues which correspond to

phonetically relevant acoustic features [55,73,108] while

the anterior part maps acoustic-phonetic cues onto lexical

and grammatical representations [82,88]. In summary, brain

regions mediating higher-level aspects of speech being

made up of complex sounds as well as meaningful semantic

and even syntactic cues can be localised within left

temporo-lateral and predominantly anterior temporal and

fronto-opercular cortex [29,73,81,83]. Based on the design

of the present study, we are not able to ascribe any

particular linguistic function to distinct subportions of the

peri-sylvian cortex. However, all regions which exhibit

stronger activity for sentences relative to laughter or sounds

have been described elsewhere as playing a relevant role

during auditory sentence comprehension [22,31,61].

4.2. Sounds

Even though the sound condition we presented in the

current study was primarily considered a nonvocal control

Fig. 6. Time course of mean event-related hemodynamic responses collected from three bilateral regions of interest in the inferior parietal lobe.

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 301

condition, we discovered interesting and novel findings

which are worth a detailed discussion. Processing nonvocal

sounds involves posterior portions of the right and the left

peri-sylvian region, namely the medial part of the primary

auditory cortex, the adjacent PT, the Ppar, and the PaOp

which all subserve auditory functions [1,38,40,43,49–

55,81,87] and can be considered part of the auditory cortex

[33,78,90]. Interestingly, in the context of the present study,

the anterior parts of the STP did not reveal selective

responses to nonvocal sounds, only the posterior structures

including the PT and adjacent sections extending into the

Ppar and the PaOp responded to the presentation of

nonvocal sounds. The planum temporale has been recently

described as a universal dcomputational hubT playing an

integrative role in sound processing [37] and housing

transient representation of temporally ordered sound

sequences without distinguishing between words and other

sounds [36]. Thus, the present data support a view which

suggests the PT as governing intrinsic spectrotemporal

features of sound [103] and which characterize the PT as

responsive but not selective to speech as it is assumed to

constitute an integrating mechanism mediating an ongoing

updating between stored and present auditory information

[69]. Alternatively, it should be mentioned that the

posteromedial compartments of human auditory cortex

have been associated with processing the location of sound

sources [60,102,113]. A recent refinement of the model by

Griffiths and Warren more specifically proposes that the

PT accesses learned representations of temporarily stored

sounds in higher cortical areas and gates spatial and

object-related information [38,101]. Here, we only used

monotonous nonvocal sounds which do not vary in

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306302

location and which are difficult to spontaneously associate

with any environmental or meaningful origin. However, it

cannot be ruled out that perception of nonvocal sounds

automatically activated a neural ensemble which normally

responds to changes in spatial and object-related cues to end

up with a reasonable interpretation of nonvocal sounds.

Corroborating evidence for our finding comes from a recent

fMRI study which investigated brain regions involved in

recognizing environmental sounds [57]. While the bilateral

posterior MTG appears to preferentially subserve semanti-

cally related environmental sounds Lewis et al. [57]

reported that bilateral regions in the posterior Sylvian

cortex including the inferior parietal cortex responded to

both environmental and unrecognizable backward sounds.

Thus, our findings accord with recent studies which

proposed a processing hierarchy in the human peri-sylvian

regions with anterolateral regions such as lateral STG and

PPol being preferentially activated by complex speech

sounds while the posteriomedial portions of the Sylvian

Fissure are more strongly attributed to the processing of the

auditory structure of complex nonspeech sounds and simple

speech sounds (phonemes) [38,55]. This suggestion over-

laps with the observation that the temporo-parietal cortex,

particularly in the right hemisphere mediates abstract sound

knowledge [25]. Our finding of bilateral activity covering

the posterior peri-sylvian cortex, the tissue deeply buried in

the posterior ascending Sylvian branch up to the parietal

operculum may additionally speak to the existence of

neurons sensitive to auditory stimulation in the inferior

parietal lobe accommodating the Ppar and the PaOp. Little

is known about the specific role of the Ppar and PaOp. Both

Ppar and PaOp have been formerly attributed to auditory

processing but have not yet been assigned to any specific

function [40,49]. At least, the Ppar partly overlaps with the

cytoarchitectonic area Tpt which has been classified as

auditory cortex [33]. Thus, the present data add to the view

that the posterior portions of the peri-sylvian region mediate

processing of fine-grained, spectro-temporal, acoustic cues

and can therefore be considered part of the auditory cortex

in man [18] even though it is not possible to precisely

identify the functional contribution of distinct subregions

(PT, Ppar, PaOp) which brought on a signal increase for

nonvocal sounds.

4.3. Laughter

Hearing laughter when compared to speech or sounds

preferentially engages the right STG including the primary

auditory cortex. This finding is in line with a recent fMRI-

study which also reported a stronger right STG involvement

in processing human laughter [80]. As speech and laughter

do not considerably differ in acoustic complexity, other

issues must account for this finding. Numerous clinical

studies pointed to a right hemisphere preference for

affective moods [13,44]. However, contradictory evidence

comes from a view which claims that the right hemisphere

does not universally process affective moods [96]. It rather

seems that the right hemisphere is more proficient in

processing acoustic cues such as changes in pitch, ampli-

tude, and frequency modulations if they load affective

information. Vice versa, linguistically loaded changes in the

same acoustic parameters may preferentially drive the left

hemisphere. As laughter is an affective utterance, it is

plausible that the right auditory cortex exhibits a starker

involvement.

One may have assumed that laughter also may have

evoked responses in other demotionally drivenT system

involving the amygdala, thalamic/hypo-, and subthalamic

areas proposed by Wild et al. [105]. We believe that the

laughter sequences we used in the present study were not

sufficient to induce considerable emotional sensations for

two reasons. First, the laughing samples were recorded

from professional actors. After scanning, volunteers

reported that they did not perceive the laughing samples

as dcontagious laughterT in any case. However, Sander and

Scheich [80] also used laughing recorded from professional

actors as stimuli. Unlike our study, they observed clear

brain responses in the amygdala to laughing and crying.

Notably, Sander and Scheich used continuous streams of

laughter which lasted ten times longer than the laughing

sequences we applied in our study. Therefore, it is plausible

that this difference in duration accounts for the differences

in results.

Additionally, laughter produced activation in the right

subcentral gyrus and precentral gyrus which has been

described as part of the dvoluntaryT system partly constitut-

ing the neural basis of expressive laughter in the brain. It is

therefore conceivable that hearing laughter also excites

brain regions which belong to the neural circuit subserving

expressive laughter [79]. Analogously, brain regions which

support the production of speech also appear to be involved

in speech processing [24,48,64,106].

4.4. Vocal timbre—the potential role of the (right posterior)

STG

The design of the present study also enabled us to

perform a particular post hoc conjunction analysis to

identify regions which commonly activate during both

perception of speech and laughter, that is, human vocal

timbre which could be considered the most prominent

acoustic feature which distinguishes between vocal and

nonvocal sounds. In the view of the present results, the right

and left anterior lateral STG preferentially responded to

stimuli made up of vocal timbre with the right hemisphere

playing a considerably stronger role. Furthermore, the

medial compartment of HG lining the posterior insular

cortex also activated saliently during vocal timbre percep-

tion. This strong asymmetry conflicts with at least one

recent PET study which concluded that temporal brain

structures we observed to respond more strongly to vocal

timbre (mid STG/HG) are functionally symmetrical [93].

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306 303

However, this study by Tzourio-Mazoyer et al. did not

explicitly investigate the significance vocal information may

have for the right hemisphere. Corroborating evidence

which lends credence to our view comes from a multitude

of clinical and brain imaging studies. For decades, the study

of neurologically impaired patients was the only source of

information about the neural processing of voices. Evi-

dently, our findings agree with the former neuropsycho-

logical research as these clinical observations suggest that

lesions of the temporal lobe of either hemisphere may lead

to deficits in the discrimination of unfamiliar voices

[95,97,98]. Apparently, a lesion in the right hemisphere

only leads to a deficit in the recognition of familiar voices

[95]. Recently, the neural processing of voice information

has also been particularly investigated by functional

imaging experiments corroborating and complementing the

clinical data. In a recent functional magnetic resonance

imaging (fMRI) study [99], it was shown that a task

targeting on the speaker’s voice (in comparison to a task

focussing on verbal content) leads to a response in the right

anterior superior temporal sulcus of the listener. In another

series of studies [6,7], it was shown that temporal lobe areas

in both hemispheres responded more strongly to human

vocal timbre than to other vocal sounds, such as bells, dog

barks, machine sounds with the right anterior polymodal

STS being preferentially driven by human vocal information

[4,8,36,56,100]. We also observed activation at the fund of

posterior STS when volunteers heard vocal timbre relative

to sounds. We presume that differences in baselines used in

the different studies may account for the different STS

locations.

Admittedly, the picture on vocal timbre perception

remains fragmentary, but this post hoc conjunction analysis

is at least in harmony with a host of clinical and

neuroimaging studies which describe the superior temporal

lobes as eminently relevant brain structures for the

perception of human vocal information.

When compared to nonvocal sounds, vocal timbre

produced activity in the left and right fusiform gyrus.

Cross-modal mechanisms may account for this intriguing

result. Previous observations in normal-hearing subjects and

in patients with cochlear implants have established that

visual cortex participates in speech processing [35], in

particular when listening to meaningful sentences [34]. The

precise location of activity in visual areas evoked by

auditory stimuli varies across studies. Giraud et al. observed

activity in the vicinity of the fusiform face area while

cochlear-implant patients were listening to speech [34]. The

authors suggest that patients probably translated auditory

speech into facial expressions. Therefore, it is not unlikely

that participants in the present study mentally associated a

laughing or speaking face, while hearing speech and

laughter. More corroborating evidence comes from an fMRI

study which reports fusiform and lingual activity collected

while participants heard sentences [99]. In the line of the

authors, these results imply that participants translated

auditory information into specific visual representations to

better accomplish the task. Interestingly, the same cross-

modal interaction works vice versa as it has been

demonstrated that seeing speech recruits auditory areas

[17,59]. Due to our results hearing nonvocal sounds did not

evocate internal images and therefore did not produce

activity in areas associated with imagery of faces.

Generally, the data allow us to draw the following picture

sketching a functional division of the peri-sylvian cortex.

Regions in the PAC and the peri-auditory cortex appear to

be proficient at integrating complex spectro-temporal

signals even though our data suggest a functional asymme-

try varying with global and temporal information available

in acoustic stimuli. Once the inflowing acoustic signal has

been identified as spoken language, regions in the antero-

lateral and posteriolateral STG, particularly in the left

hemisphere, initiate fine-grained processing at the phonetic,

semantic, and syntactic level. If auditory input does not

entail any speech, speech-like, or even vocal information

regions in the posterior Sylvian region and the inferior

parietal lobe become involved in acoustic analysis. Unlike

vocal environmental sounds (dog barks, baby cries), the

nonvocal sounds used in the present design cannot easily be

associated with any meaning. It is therefore plausible to

assume that enlarged activity for sounds reflect the search

for a sensible interpretation. Recent observations underline

this notion of the posterior peri-sylvian cortex as being

highly sensitive to all categories of meaningful and mean-

ingless complex sounds [87].

5. Conclusion

In conclusion, we have delineated distinct regions in

the human peri-sylvian cortex which appear to preferen-

tially support the processing of human laughter, speech,

and nonvocal sounds. Hearing human laughter preferen-

tially involves auditory and somatosensory fields primarily

in the right hemisphere. Our findings deliver novel insight

in that it appears that hearing laughter activates the same

areas which have formerly been attributed to expressive

laughter. Hearing spoken sentences activates left anterior

and posterior lateral temporal and left inferior frontal

regions which is confirmatory with numerous former

findings. Hearing nonvocal sounds most strongly recruits

bilateral areas in the medial portion of Heschl’s gyrus and

at the medial wall of the posterior Sylvian fissure (planum

parietale) even including the inferior parietal lobe (parietal

operculum) and therefore adds functional evidence to the

ongoing debate on the extension of auditory fields in the

human brain. A post hoc conjunction analysis to identify

regions which commonly activate during both speech and

laughter revealed a functional rightward preference of

supratemporal sites for human vocal timbre. In summary,

the data add to recent work which provided evidence for a

hierarchical processing system in the peri-sylvian cortex

M. Meyer et al. / Cognitive Brain Research 24 (2005) 291–306304

with the posteriomedial region mediating acoustic proper-

ties of nonvocal sounds and anteriolateral parts of the

STG and STS supporting the perception of human vocal

timbre.

Acknowledgments

The authors wish to thank Lutz Jancke, Adam McNa-

mara, and two anonymous reviewers for helpful comments

on the manuscript.

During the preparation of the manuscript, Martin Meyer

was supported by Schweizer National Fonds (Swiss

National Foundation) SNF 46234101, dShort-term and

long-term plasticity in the auditory systemT. This study

was also supported by the project AL 357/2-1 by the

Deutsche Forschungsgemeinschaft (German Research

Foundation, DFG) as well as by the Human Frontier

Science Program (HFSP RGP5300/2002-C102) awarded

to Kai Alter.

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