what and where in auditory space

SPECIAL ISSUE
AUDITORY NEGLECT: WHAT AND WHERE IN AUDITORY SPACE
Stephanie Clarke and Anne Bellmann Thiran
(Division de Neuropsychologie, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland)
ABSTRACT
A sound that we hear in a natural setting allows us to identify the sound source and to localise it in space. Several lines
of evidence indicate that the two aspects are processed in anatomically distinct cortical networks. Auditory areas that are
part of the What or Where processing streams have been identified recently in man and in non-human primates. Comparison
between anatomical and activation studies suggests that processing within either stream can be modulated by specific
attentional factors.
Attending to auditory events can be affected in neglect. Bisiach et al. (1984) described systematic directional errors to
the ipsilesional space, which was considered a manifestation of hemispatial neglect and interpreted as a disruption of the
neural network providing the internal representation of egocentric space. The other manifestation of auditory neglect is
contralesional extinction in dichotic listening condition (Heilman and Valenstein, 1972). Recently two types of auditory
neglect have been described, one corresponding to a primarily attentional deficit associated with basal ganglia lesions and
the other to distortions of auditory space representations associated with parieto-prefrontal lesions (Bellmann et al., 2001).
Based on studies of sound detection and sound recognition following hemispheric lesions we argue that the two types of
neglect correspond to disturbed processing in either the What or the Where stream.
Key words: spatial processing, sound recognition, auditory cortex, auditory attention
INTRODUCTION
Bisiach is one of the few authors who have
initiated the investigation of auditory spatial
functions in man. He and his colleagues have
assessed auditory localisation by means of a
stereophonic test simulating spatial lateralisations
by interaural intensity differences, and found
systematic directional errors to the ipsilesional
space (for left-sided as well as right-sided targets)
in right-damaged patients (Bisiach et al., 1984).
This auditory spatial bias after right-hemispheric
damage, also documented in two other studies of
the same group (Vallar et al., 1995, Sterzi et al.,
1996), was considered a manifestation of
hemispatial neglect and interpreted as a disruption
of the neural network providing the internal
representation of egocentric space. This
interpretation is in line with the general concept of
neglect as a distortion of represented space, with
compression on the ipsilesional side and expansion
on the contralesional, defended by Bisiach and
collaborators (Bisiach et al., 1996; 1998a; 1998b).
In the visual modality, this concept has been
classically opposed to the ‘attentional’ theories of
neglect (e.g. Mesulam, 1981).
The ability to acknowledge the presence of an
object must be distinguished from the ability to
localise this object with respect to one’s own body.
This notion can be related to the now well
established dichotomy, within the visual system,
between a ventral stream involved in object
processing, and a dorsal stream dedicated to spatial
localisation and to action in space. Some authors
Cortex, (2004) 40, 291-300
have relied on this model to explain different
aspects of visual neglect: Humphreys (1998) argues
that between-objects and within objects are
differently mediated by the dorsal and ventral
pathways, while Farah and collaborators develop
the idea of an ‘object-based’ attention and a
‘location-based’ attention (Farah et al., 1993; Farah
and Buxaum, 1997). The role of multiple
representations of space, sustained by the parietal
cortex, and their breakdown in visual extinction
and neglect are stressed in a recent review by
Marshall and Fink (2001).
The purpose of this paper is to consider the
actual situation of auditory neglect in the light of
recent investigations of the anatomical and
functional organisation of the human auditory
cortex. The evidence favouring the existence of a
ventral network dedicated to the recognition of
auditory objects, and a dorsal network involved in
the processing of the auditory spatial dimension of
these objects will be reviewed. We shall argue that
auditory neglect phenomena are at least partially
related to one of these two auditory networks: a
neglect within the dorsal network will lead to
spatial bias in auditory localisation, whereas an
auditory neglect in the ventral stream will manifest
itself by inter-object omissions.
WHAT AND WHERE PROCESSING STREAMS
IN HUMAN AUDITION
A sound that we hear in a natural setting allows
us to identify the sound source and to localise it in
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Stephanie Clarke and Bellmann Thiran
space. Several lines of evidence indicate that the
two aspects are processed at the cortical level
independently in anatomically distinct neural
networks.
Activation Studies
Direct comparisons of networks involved in
sound recognition and sound localisation were
reported recently and confirmed their anatomical
segregation. We have investigated activation
associated with performance in sound identification
and sound localisation in normal subjects with
fMRI using three conditions: i) comparison of
spatial stimuli simulated with interaural time
differences; ii) identification of environmental
sounds; and iii) rest (Maeder et al., 2001; Figure
1A).
Conditions
i)
and
ii)
required
acknowledgement of predefined targets by pressing
a button. Sound recognition and sound localisation
activated, as compared to rest, inferior colliculus,
medial geniculate body, Heschl gyrus and parts of
the temporal, parietal and frontal convexity
bilaterally. The activation pattern on the frontotemporo-parietal convexity differed in the two
conditions. Middle temporal gyrus and precuneus
bilaterally and the posterior part of left inferior
frontal gyrus were more activated by recognition
than by localisation. Lower parts of inferior
parietal lobule and posterior parts of middle and
inferior frontal gyri were more activated,
bilaterally, by localisation than by recognition.
Passive listening paradigm revealed segregated
pathways on superior temporal gyrus and inferior
parietal lobule. Alain et al. (2001) used an S1-S2
match-to-sample task in which S1 differed from S2
in its pitch and/or location. Relative to location,
pitch processing generated greater activation in
auditory cortex and the inferior frontal gyrus.
Conversely, identifying the location of S2 relative
to S1 generated greater activation in posterior
temporal cortex, parietal cortex, and the superior
frontal sulcus. This study demonstrated also a
dichotomy between localisation and recognition
processing. The What stream was, however, only
partially visualised, probably due to a task which
did not require the identification of sound objects.
A functional segregation of the What and Where
processing streams was further confirmed by
electrophysiological studies using pitch localisation paradigms (Alain et al., 2001;
Anourova et al., 2001).
These direct demonstrations of the What and
Where processing streams are in agreement with
previous activation studies which compared
activation to a recognition task vs. rest or to a
spatial task vs. rest. Categorisation of
environmental sounds, involving recognition, was
shown to activate specifically left prefrontal,
temporal, parietal and cingulate regions (Engelien
et al., 1995). Sound localisation was shown to
activate largely distributed cortical networks with
an important contribution of the temporal, parietal
and prefrontal cortices (Griffiths et al., 1998; 2000,
Bushara et al., 1999, Maeder et al., 2001). The
activation by auditory spatial stimuli was bilateral
in all studies, but some authors suggested a
dominance of the right hemisphere (Griffiths and
Green, 1999; Weeks et al., 1999; Griffiths et al.,
2000), whereas others found no evidence for
lateralisation in auditory spatial processing
(Bushara et al., 1999, Woldorff et al., 1999).
Auditory Short-term Memory
Distinct neural populations sustain also shortterm memory for sound content and sound
localisation. We have investigated the role of
auditory or visual interference tasks in a
same/different comparison of two sound stimuli
separated by an interval in normal subjects (Clarke
et al., 1998). Auditory interference tasks reduced
memory for sound content and sound location in a
specific way. Memory for sound content was
significantly more reduced by auditory recognition
than by auditory spatial interference tasks. Visual
interference tasks significantly reduced memory for
sound location but not for sound content. These
results suggest that short-term memory for sound
content and that for sound location involve
partially distinct processing, and auditory spatial
functions are more closely linked to visual
functions than auditory recognition.
Effects of Focal Lesions
The dichotomy of auditory What and Where
processing streams, as demonstrated in normal
subjects, predicts that focal lesions, centred on one
or the other network are associated with the
corresponding selective deficits. This has been
suggested by published case studies: 3 cases of
auditory agnosia without auditory localisation
deficits (Spreen et al., 1965; Jerger et al., 1972;
Fujii et al., 1990) following right or bilateral
lesions; and 1 case of selective impairment of
auditory motion perception following a right
hemispheric lesion that included the insula and
parietal convexity (Griffiths et al., 1996; 1997).
A recent study of 15 consecutive patients with
right focal hemispheric lesions showed that sound
recognition and sound localisation can be disrupted
independently (Clarke et al., 2002). In this series, 4
patients were normal in sound recognition but
severely impaired in sound localisation, whereas 3
other patients were deficient in recognising sounds
but localised them well. The lesions involved the
inferior parietal and frontal cortices, and the
superior temporal gyrus in patients with selective
sound localisation deficit; the temporal pole and
anterior part of the fusiform, inferior and middle
temporal gyri in patients with selective recognition
Auditory neglect
A
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Selective deficit in auditory recognition (N=3)
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Fig. 1 – Cortical networks involved in sound recognition and sound localisation. A: Mean activation of 18 normal subjects; green
denotes regions activated more by sound recognition than sound localisation and red regions activated more by sound localisation than
sound recognition (adapted from Maeder et al., 2001). B: Superimposed right-hemispheric lesions associated with selective deficit in
sound localisation (left; four patients) or selective deficit in sound recognition (right; three patients). The lesions are represented in
Talairach space, sections c and D. Hatching indicates the number of patients in whom a given Talairach cube was damaged (adapted
from Clarke et al., 2002).
deficit (Figure 1B). This double dissociation clearly
supports conclusions drawn from activation and
electrophysiological studies (Maeder et al., 2001;
Alain et al., 2001; Anourova et al., 2001).
Selective deficits in sound recognition or sound
localisation were also found in cases with unilateral
left hemispheric lesions (Clarke et al., 2000). In
this series, 1 patient was severely deficient in
recognition of environmental sounds but normal in
auditory localisation and auditory motion
perception. The lesion included the left superior,
middle and inferior temporal gyri and lateral
auditory areas, but spared Heschl’s gyrus, the
acoustic radiation and the thalamus. Another
patient, with the same profile, had a lesion that
comprised the postero-inferior part of the frontal
convexity and the anterior third of the temporal
lobe. A third patient was severely deficient in
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Stephanie Clarke and Bellmann Thiran
auditory motion perception and partially deficient
in auditory localisation, but normal in recognition
of environmental sounds; the lesion involved large
parts of the parieto-frontal convexity and the
supratemporal region. These cases confirm that
lesions of the What or the Where processing
streams in the left hemisphere cause the
corresponding deficits.
EVIDENCE
FROM
A
NON-HUMAN PRIMATES
Auditory What and Where processing streams
have been demonstrated anatomically and
functionally in non-human primates. Macaque
auditory cortex is subdivided into three sets of
areas called core, belt and parabelt; individual
areas were defined by electrophysiological and/or
architectonic criteria (for review see e.g.
Rauschecker et al., 1998; Kaas et al., 1999). The
lateral belt areas, situated on the inferior lip of the
sylvian fissure and the supero-posterior part of the
superior temporal gyrus, tend to respond to
complex sounds corresponding to monkey calls
and/or to spatial locations. While area ML shows
specialisation for either type of information, AL
appears more specialised for monkey call-like
stimuli and CL for locations (Recanzone et al.,
2000; Tian et al., 2001). AL has been proposed to
be part of the auditory stream that subserves sound
recognition (the What stream) and CL of the
stream that subserves sound localisation (the Where
stream; Rauschecker and Tian, 2000).
HUMAN AUDITORY AREAS,
WHAT AND WHERE PROCESSING STREAMS
AND ATTENTIONAL MODULATION
A similar functional specialisation of nonprimary auditory areas was demonstrated in man.
Cytoarchitectonic criteria were used to identify 2 to
6 areas outside the primary auditory cortex,
(Brodmann, 1909; von Economo and Koskinas,
1925; Galaburda and Sanides, 1980). More recent
histochemical studies visualising cytochrome
oxidase and acetylcholinesterase activities revealed
several auditory areas: lateral (LA), superior
temporal (STA), posterior (PA), and medial (MA)
area (Rivier and Clarke, 1997; Wallace et al., 2002:
Fig. 2A). This approach, combined with the
visualisation of calcium-binding protein reactivity,
revealed also a hierarchical organisation (Mesulam
and Geula, 1994; Hustler and Gazzaniga, 1996;
Rivier and Clarke, 1997; Hackett et al., 2001;
Wallace et al., 2002; Chiry et al., 2003), which is
further supported by a recent study of intrinsic
connectivity of the human auditory cortex (Tardif
and Clarke, 2001). In particular, three levels were
distinguished: a first level corresponding to the
primary auditory area; a second level with four
B
“Where”
“What”
Level III
Level II
Level I
Fig. 2 – A. The position of auditory areas on the human
supratemporal plane (AI, LA, PA, MA, AA and STA) as defined
by patterns of cytochrome oxidase and acetylcholinesterase
activity (Rivier and Clarke, 1997). Scales indicate Talairach coordinates (Talairach and Tournoux 1988). B. Schematic
representation of What and Where auditory processing streams
based on anatomical (Rivier and Clarke, 1997; Tardif and
Clarke, 2001; Wallace et al., 2002; Chiry et al., 2002) and
activation studies. Horizontal hatching denotes areas shown to
be selectively activated by sound recognition-type processing
(LA, STA; Hall et al., 2002) and crossed hatching areas located
in the posterior part of the planum temporale, shown to be
involved in spatial processing (Weeks et al., 1999; Warren et al.,
2002). Asterisks mark areas shown to have increased activation
by attention-related factors, STA more than LA and PA
(Hashimoto et al., 2000).
areas (LA, MA, PA, AA; Figure 2B) and a third
level with at least one area (STA). The
heterogeneity of parvalbumin and calbindin
expression within the four early stage areas
suggested that they may belong to different
processing streams, areas LA and STA to the What
stream, and areas MA and PA to the Where stream
(Figure 2B; Chiry et al., 2003).
Such an organisation is supported by activation
studies, which demonstrated a specialisation for
sound recognition-type processing in non-primary
areas situated laterally and anterolaterally to the
primary cortex, and specialisation for auditory
spatial processing in postero-medial areas.
Frequency modulation was shown to increase
activation within areas LA, STA and a region
anterior to AA, but not in AA, MA and PA (Figure
2B; Hall et al., 2002). More generally, stronger
activation by complex stimuli was found in belt
Auditory neglect
areas than in the primary auditory cortex
(Wessinger et al., 2001). Anterior part of the
superior temporal gyrus (on the left side) was
activated in speech processing (Binder et al.,
2000). Posterior part of the superior temporal gyrus
and the planum temporale were found to be
involved in spatial processing (Figure 2B; Weeks et
al., 1999; Warren et al., 2002).
Non-primary auditory areas have been shown to
be specialised either in sound recognition or sound
localisation and constitute thus the early stages of
the What and Where processing streams. It is
interesting to note that some of these areas may be
specifically modulated by attentional load. This has
been demonstrated by an activation study using
dichotically or diotically presented speech stimuli
(Hashimoto et al., 2000). Diotic was defined by
these authors as the presentation of the same
stimulus (without interaural time difference) in
both ears, and dichotic as the simultaneous
presentation of two different stimuli, one in each
ear. The latter task was the more difficult one and
required greater attentional resources. Areas PA,
LA and STA showed greater responses under
dichotic than diotic condition, which was
interpreted as reflecting the increased attentional
load. Furthermore, stronger effects of attentional
modulation were observed in area STA than in
areas LA or PA (Hashimoto et al., 2000),
suggesting a hierarchical organisation, which is
very similar to that revealed by anatomical studies
(Figure 2B; Rivier and Clarke, 1997).
Discrete attentional modulation within the What
and Where processing streams may be the basis of
different types of auditory neglect which were
observed following right hemispheric lesions.
IN THE
AUDITORY NEGLECT
WHAT AND WHERE SYSTEMS
Two different types of deficits have been
attributed to auditory neglect. One manifestation of
auditory neglect is the presence of systematic
directional errors in sound localisation, including
alloacusis from the contralesional to the ipsilesional
hemispace, in tasks of overt single sound
localisation or of determination of auditory
subjective straight ahead (Altman et al., 1979;
Bisiach et al., 1984; Vallar et al., 1995; Sterzi et
al., 1996; Haeske-Dewick et al., 1996; Soroker et
al., 1997; Kerkhoff et al., 1999; Bellmann et al.,
2001). There is general agreement to consider this
type of errors as manifestation of neglect, and to
attribute them to a distortion of represented space
(Bisiach et al., 1984; Bellmann et al., 2001). Most
of these studies have raised the question of the
relationship between systematic directional errors
in the auditory modality and visual neglect and
found significant correlation, though a few cases of
dissociations have been reported (Bisiach et al.,
295
1984; Soroker et al., 1997, Kerkhoff et al., 1999).
A recent study reports also auditory disturbances
along the vertical dimension, suggesting a complex
disorganisation of the auditory space in visual
neglect (Pavani et al., 2002).
The other manifestation of auditory neglect
commonly described is contralesional extinction
(Heilman and Valenstein, 1972; Hugdahl and
Wester, 1994). It is generally observed when two
stimuli are simultaneously lateralised in the
auditory space. Dichotic listening is the procedure
most often used to display two different
simultaneous stimuli. It remains, however, disputed
how far dichotic extinction reflects a primary
attentional deficit and is thus appropriate for the
diagnosis of auditory neglect (Beaton and
McCarthy, 1995). An alternative interpretation
considers extinction as a consequence of defective
transmission or processing of the sensory stimuli
delivered from the ear having privileged links to
the lesioned hemisphere (Kimura, 1967; Sparks and
Geschwind, 1968; De Renzi et al., 1984; Beaton
and McCarthy, 1995). In a recent study, we have
circumvented the interpretation impasse proper to
the dichotic procedure, by lateralising each of the
two stimuli by an interaural time difference (ITD)
of 1 msec favouring the left ear in one case and
the right ear in the other case. An illusion of
double lateralisation similar to that encountered
with the dichotic procedure was thus created (one
stimulus perceived to the left, the other
simultaneously to the right), but without any
difference in the intensity level and content
received by each ear. With this task, we were able
to document contralesional omissions in condition
of double stimulation, which were clearly
attributable to auditory spatial neglect. These
results confirmed data reported by other authors
who used free-field presentations by means of two
lateralised loud-speakers (Tweedy et al., 1980;
Soroker et al., 1997; Deouell and Soroker, 2000).
These two different profiles of auditory neglect,
i.e., systematic directional errors in sound
localisation versus contralesional omissions when
an ipsilesional stimulus is simultaneously
presented, were found to double dissociate in cases
of right-hemispheric lesions. We have assessed
auditory neglect with a task of sound localisation
(by means of ITD simulations) and with an ITD
diotic listening task in four right-damaged patients
(Bellmann et al., 2001). Two patients (JCN and
MB) presented a marked hemispatial asymmetry
favouring the ipsilesional hemispace in the ITD
diotic test, but did not show any spatial bias in
sound localisation. Two other patients (AJ and ES)
had the reverse profile: no hemispatial asymmetry
in the ITD diotic test, but a severe spatial bias
directed to the ipsilesional side in sound
localisation (Figure 3). JCN and MB had mainly
subcortical lesions affecting basal ganglia. AJ and
ES had cortical lesions in the prefrontal, superior
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Stephanie Clarke and Bellmann Thiran
A
B
Fig. 3 – Two types of auditory neglect. Four patients (JCN, MB, AJ, ES), with right hemispheric lesions and left ear extinction on
dichotic listening task, presented different profiles in auditory spatial attention versus auditory localisation tests. A. Asymmetry on the
diotic listening test as compared to controls (mean value of the control population is indicated by CTRL, limit of normal performance by
the dotted line). JNC and MB, but not AJ and ES, presented extinction of sound stimuli presented within the left hemispace. B. Sound
localisation of positions simulated with interaural time differences of 1 ms (LL) or 0.3 ms (L) in favour of the left ear, 1 ms (RR) or 0.3
ms (R) in favour of the right ear or without interaural time difference (C). JCN and MB performed as normal controls (not shown here),
while AJ and ES had a rightward bias in their performance.
temporal and inferior parietal areas. These results
suggest the existence of two functionally and
anatomically distinct types of auditory neglect: i)
contralesional omissions in condition of double
stimulation, following lesions centred on basal
ganglia; or ii) ipsilesional spatial bias following
fronto-temporo-parietal lesions.
The dissociation between these two types of
auditory neglect is not rare. It was found in 40% of
cases in a series of 15 consecutive patients with
right unilateral hemispheric lesion entering our
rehabilitation programme (Bellmann et al., 2001;
Bellmann, 2001; Bellmann Thiran and Clarke,
2003). Although the role of basal ganglia in neglect
is supported by anatomo-clinical correlations (Hier
et al., 1977; Damasio et al., 1980; Healton et al.,
1982) and by the relative success of dopaminergic
treatment (Fleet et al., 1987; Geminiani et al.,
1998; Hurford et al., 1998; Mukand et al., 2001),
their specific involvement in the attentional type of
auditory neglect needs to be further investigated.
The manifestations of the two types of auditory
neglect described above occurred in very different
situations. In the localisation task, subjects had to
process one given object at a time, whereas in the
ITD diotic task, two simultaneous sounds were
provided together. As emphasised already by Efron
et al. (1983) and demonstrated in dichotic listening
Auditory neglect
tasks (Hugdahl and Wester, 1994), contralesional
omissions of single sound targets are very rare.
Further evidence of dissociation between the
processing of one versus multiple objects in the
auditory modality has been provided by Cusack
and collaborators (2000). They reported betweenobjects attention deficits without within-object
attention deficit in patients suffering from visual
hemineglect1. The authors concluded that withinobject
comparisons
and
between-objects
comparisons are separately represented in the
auditory modality as well as in the visual modality.
In the study of Cusack and collaborators, the sound
objects followed each other in the temporal and not
the spatial dimension as in our study. This suggests
that attentional mechanisms (not necessarily
spatial) are involved when multiple objects have to
be processed. Interestingly, theories of visual
neglect elaborated on the basis of studies on
extinction have generally advocated an asymmetry
between the attention allocated to the right vs. left
hemi-spaces and/or a reduction in processing speed
or capacity (Di Pellegrino and De Renzi, 1995;
Driver et al., 1997). In line with these propositions,
it has been found that patients with left-sided
extinction perceived ipsilesional visual events
earlier than physically synchronous contralesional
stimuli (Rorden et al., 1997). This suggests that
these patients have a chronic bias of spatial
attention towards the ipsilesional side, and that
stimuli occurring at that attended location are
processed more rapidly and receive privileged
access to awareness. This phenomenon of ‘prior
entry’ has recently been found in the auditory
modality (Karnath et al., 2002). These attentional
theories contrast with conceptions of hemispatial
neglect as a distortion of egocentric space
representation (Bisiach et al., 1996; 1998a; 1998b;
Karnath, 1997), which are particularly convincing
to explain directional spatial bias in tasks where
only one ‘object’ is processed at the same time (for
example: line bisection, Milner’s landmark task,
straight ahead pointing). The differential
involvement of attention may thus underlie, at least
partially, the dissociations between contralesional
extinction and other forms of neglect, documented
in the visual (Barbieri and De Renzi, 1989; Di
Pellegrino and De Renzi, 1995) and auditory
modality (Bellmann et al., 2001).
The sound localisation and ITD diotic tasks also
differ along another dimension. In the first case,
the subjects are explicitly required to attribute a
spatial co-ordinate to the sound target. In the
second case, they are instructed to acknowledge
and report the content of the information contained
in the auditory field. We have reviewed above the
growing evidence that the dichotomy between a
1The
respective involvement of the What and Where processing streams has
not been determined in these cases and further studies with precise
anatomoclinical correlations are needed.
297
dorsal-spatial system and a ventral-object system
also exists in the auditory modality. Other authors
have tried to relate auditory neglect to this
organisation of the auditory system (Soroker et al.,
1995; Deouell and Soroker, 2000; Cusack et al.,
2000). For instance, Soroker and collaborators
(1995) have shown that extinguished verbal stimuli
delivered through a loudspeaker on the left side
could be reinstated if a fictitious loudspeaker was
visible on the right, ipsilesional side. They
interpreted the extinction phenomenon as a
disconnection between the ‘Where’ system and the
‘What’ system (which could identify the target but
was unable to locate it). The presence of a rightsided potential ‘where’ target would allow the
processing of the information. Similar ability of
right-damaged patients to identify left-targets that
were mislocalised to the right side of space has
been demonstrated more recently by the same
group (Deouell and Soroker, 2000).
The directional bias observed in auditory
localisation in our study and by others can clearly
be related to a distortion error within this dorsal
system. The cerebral lesions responsible for this
behaviour are also compatible with the dorsal
auditory network revealed by functional studies
(Maeder et al., 2001; Warren et al., 2002). They are
mainly located in the right parietal lobe (Bisiach et
al., 1984; Vallar et al., 1995; Sterzi et al., 1996;
Haeske-Dewick et al., 1996) or in the right parietofronto-temporal region (Bellmann et al., 2001).
The dichotic or diotic tasks have more links
with the ventral system: they do not require overt
space processing, the instruction being oriented to
the analysis of the content of information. There is
however a spatial component in the fact that the
extinction is spatially lateralised. We shall argue
below that a part of spatial processing is dedicated
to the What system.
Psychophysical studies in normal subjects
suggest two different roles for auditory spatial
cues. One is auditory localisation, i.e. the ability to
attribute precise egocentric spatial co-ordinates to a
sound, involving overt perception of sound
location. Auditory spatial information can also be
used as a cue for sound object segregation, also
referred to as ‘auditory streaming’ (Bregman, 1990;
Yost, 1991) or ‘cocktail party effect’ (Cherry,
1953). Spatial cues facilitate the grouping of sound
components that belong to the same sound object
and the distinction from other sound objects.
Segregation of sound objects contributes thus
decisively to sound recognition in noisy
environment. Efron and collaborators have
proposed the existence of a ‘temporal lobe
enhancement mechanism’ whose function is to
facilitate perception of sound sources located in the
opposite side of space when other sounds are
present throughout the auditory field. They found
that this ‘cocktail party’ competence was impaired
in the hemi-space contralateral to a temporal
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TABLE I
Relationship between Processing within Auditory What and Where and Neglect
What stream
Type of spatial processing
Role of spatial processing
Manifestation of neglect
Process underlying neglect
Sound object segregation
Facilitation of perception
Contralesional omissions
Attentional
lobectomy (Efron et al., 1983). Carlyon and
collaborators have described less stream
segregation of tone sequences presented to the left
than to the right ear of patients suffering from
unilateral neglect (Carlyon et al., 2001). We have
investigated sound localisation and spatial
segregation of sound objects in a patient (NM) who
complained of difficulties in localising sounds in
everyday life after a right temporo-parieto-frontal
ischemic lesion (Bellmann et al., 2003). Two
groups of tasks were used, in which spatial
dimension was simulated by interaural time
difference (ITD): i) active localisation of stationary
or moving sound targets, and ii) sound segregation
on the basis of spatial cues. The latter included a
spatial-release-from-masking paradigm and two
ITD diotic tasks. NM failed to localise stationary
and moving sounds: she perceived all the stimuli at
the centre of the head, and could not differentiate
stationary from moving targets. In contrast, NM
was able to use ITD cues to segregate simultaneous
sound sources in the spatial-release-from-masking
paradigm and in ITD diotic tasks. These results
suggest that sound localisation and sound object
segregation based on spatial cues do not rely on
the same mechanisms.
We have thus described so far two different and
at least partially independent uses of spatial cues,
one implemented in the Where system, aimed to
provide a precise spatial description and allow
oriented responses to a sound target, the other at
the service of the What system, involved in the
segregation of simultaneous sound sources to
facilitate perception. Neglect can be considered a
high-level process which operates upon preliminary
spatial processing (either localisation or
segregation). We propose that each of the two
types of neglect described above, i.e.,
contralesional omissions and directional errors, is
more intimately linked with one form of auditory
processing. Neglect of left-sided sound sources
presented simultaneously with right-sided sources,
can occur only if sound sources have been spatially
segregated from each other. Alain and Arnott
(2000) have argued that the ability to focus
attention selectively on a particular sound source
depends on a preliminary analysis that partitions
the auditory input into distinct perceptual objects.
Previous electrophysiological studies on sound
object segregation have shown that these
mechanisms occur at a pre-attentive level (Sussman
et al., 1999; Yabe et al., 2001). The other type of
Where stream
Sound localisation
Orientation to the sound
Directional errors
Distorted spatial representation
auditory neglect (directional errors) is clearly
linked to the Where system. For example, the
alloacusis displayed by the patient AJ occurred
only for extreme left stimuli (the more central leftsided stimuli were correctly set in the left hemispace). This suggests that the bias operated on a
prior analysis of the spatial position.
In summary, there is increasing evidence that
processing within the auditory What and Where
networks can be differentially affected in neglect
(Table I). The ventral network is dedicated to the
analysis of stimulus content and the dorsal to that
of spatial position with respect to the body. In the
auditory modality, spatial aspects are computed on
the basis of monaural spectral cues or interaural
differences in time or intensity level. These spatial
cues serve, however, different goals. The most
obvious is overt localisation of sounds with respect
to the own body, implemented in the Where
system. These spatial cues are, however, also used
by the What system to help segregate simultaneous
sound sources to facilitate perception in noisy
environment. We propose that different types of
auditory neglect may reflect disturbed attentional
processing within the What and Where systems.
The neglect type which we propose involves the
What system is characterised by contralesional
omissions in situations of between-objects
comparisons, once objects have been partitioned by
pre-attentive segregation processes; it occurs after
basal ganglia lesions. The deficit is likely to be due
to a spatio-attentional disorder, i.e., different
allocation of attention between the left and right
half of the space, eventually associated with a
reduction of processing speed or capacity. The
neglect type which we propose involves the Where
system is characterised by directional errors
towards the ipsilesional hemi-space after temporoparieto-frontal cortical lesions. The deficit is likely
to be due to distortion of the represented space
rather than attentional disorder.
Acknowledgements. This paper was supported by the
Swiss National Science Foundation grant 3100-064085.00
and by the Lausanne Medical Faculty RATP grant.
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Stephanie Clarke, Divisione de Neuropsychologie, CHUV, 1011 Lausanne.
e-mail: Stephanie.Clarke@chuv.hospvd.ch