Auditory processing -- speech, space and auditory objects
Sophie K Scott
There have been recent developments in our understanding of
the auditory neuroscience of non-human primates that, to a
certain extent, can be integrated with findings from human
functional neuroimaging studies. This framework can be used
to consider the cortical basis of complex sound processing in
humans, including implications for speech perception, spatial
auditory processing and auditory scene segregation.
Addresses
Institute of Cognitive Neuroscience, University College London, 17
Queen Square, London, WC1N 3AR, UK
Corresponding author: Scott, Sophie (sophie.scott@ucl.ac.uk)
Current Opinion in Neurobiology 2005, 15:1­5
This review comes from a themed issue on
Cognitive neuroscience
Edited by Angela D Friederici and Leslie G Ungerleider
0959-4388/$ ­ see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.conb.2005.03.009
Introduction
In comparison with vision, auditory processing has tradi-
tionally been the poor relation of neuroscience. This is
partly because of the technical difficulties involved in
studying audition, both in recording from primate audi-
tory areas and in stimulus selection and presentation, and
because of the perceived dominance of vision -- a dom-
inance that neatly reverses if different tasks are used [1].
The processing demands of audition differ from those of
vision in several important ways. First, sounds only have
structure that evolves over time -- in terms of both
steady-state and changing aspects of the structure [2]
-- which potentially places different demands on the
nature of auditory `memory' [3]. Second, spatial informa-
tion in sound needs to be reconstructed from two inputs
(the binaural hearing system) [4], which has important
consequences for the neurophysiology of auditory scene
segregation. Whereas the primate auditory system solves
many of the physical problems of auditory spectral and
temporal structure and spatial organization subcortically
[5], the information also needs to be represented corti-
cally, and this probably contributes to acoustic scene
segregation [6]. Third, sounds are generated by physical
action -- be it animate or inanimate. This means that
information about actions is intimately associated with
the nature of auditory representations, which is not
necessarily the case for static visual scenes [7
]. In this
review, the cortical basis of audition in primates is con-
sidered with reference to auditory objects, scene segrega-
tion and actions. This also encompasses implications for
speech perception.
In a preceding review, Nelken [8] identified auditory
cortex as having a role in the representation of auditory
objects, rather than a role in the representation of invar-
iant acoustic cues and features. This is an especially
important suggestion because it has not been simple to
establish the role of auditory cortex in hearing -- ablating
auditory cortex does not result in cortical deafness [9].
Rather, auditory cortex seems to be necessary for com-
puting and representing complex acoustic properties of
stimuli [10
,11]. Simplistic comparisons of the auditory
cortex in humans with that in non-human primates
remain controversial. However, in this review I assume
that the general properties of non-human primate cortical
processing are sufficiently similar [12
] to those in
humans, and integrate findings from the two fields in
an attempt to find commonalities.
From sounds to speech and space
Using positron emission tomography (PET) with mon-
keys, Poremba and co-workers [13] have demonstrated
that extensive regions of primate cortex are responsive to
acoustic stimulation (Figure 1). Importantly, these areas
are located in frontal and temporal lobe regions adjacent
to visually responsive cortex, with some areas of overlap.
Within this widespread auditory system, there are now
well-established patterns of connectivity from primary
auditory cortex (PAC) (Figure 1). There are both hier-
archically organized and parallel connections from PAC to
belt and parabelt cortex, and projections from anterior and
posterior auditory fields to premotor and prefrontal cor-
tex. These connections have been expressly compared
with those of the visual system, with respect to both the
distinctive primate pattern of hierarchical organization of
sensory cortex [14] and the partially distinct (although
interacting) routes to anterior brain regions [15­17]. Simi-
lar to the situation in the visual system, there is a corre-
sponding hierarchy of functional responses to acoustic
stimulation; responses to pure tones can be observed in
PAC, and responses to sounds with progressively greater
signal bandwidths can be seen in lateral belt and parabelt.
The response in the parabelt is organized cochleotopi-
cally in a rostral­caudal direction [18
], with center
frequency reversals that resemble those seen in core
primary auditory cortical fields. There is also a functional
specialization along the rostral­caudal dimension, with
rostral parabelt regions showing an enhanced response to
CONEUR 255
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conspecific vocalizations, and caudal parabelt regions
showing greater sensitivity to the location in space of
the calls [19]. The rostral­caudal distinction can also be
seen in the response to more general properties of sounds:
rostral lateral belt regions also respond preferentially to
slower frequencymodulated(FM) sweeps, whereas caudal
lateral belt regions respond best to fast FM rates [20
].
This rostral­caudal distinction in function and anatomy
has led to the proposal that the relatively distinct streams
of processing can be fractionated along functional lines --
an anterior or rostral `what' pathway and a posterior or
caudal `where' pathway -- and that this framework can be
used to understand both lesion [21] and functional ima-
ging studies [22
] in humans. Although aspects of the
what­where distinction remain controversial [23,24], this
is a framework that has generally gained support from
human functional imaging studies. For example, posterior
auditory or inferior parietal cortical responses are consis-
tently seen across studies to sounds with spatial charac-
teristics (e.g. moving sounds) [22
], and the planum
temporale responds to speech that has a distinct free
field `outside the head' location (relative to `inside the
head') [25]. By contrast, the processing of linguistically
relevant acoustic information is associated, in humans,
with more anterior temporal lobe responses [22
]. This
pattern of hierarchical processing within an anterior­
posterior dimension has also been important in under-
standing the neural processing of speech (Figure 2; [26
]).
In this model, the `what' stream of processing, running
lateral and anterior to PAC, is progressively more respon-
sive to intelligible speech along its length (running from
posterior to anterior regions), regardless of whether or not
the speech itself sounds human in origin. This general
model has been elaborated on in more recent functional
imaging studies; whereas speech-specific responses are
not seen in PAC, a region of left superior temporal gyrus
(STG) that is lateral to PAC (and possibly corresponding
to the `parabelt' in humans) has recently been shown to
be sensitive to language-specific phonological structure
(Figure 2; [27
]). This response is left lateralized, and
might represent the start of the processing of speech
information in the anterior `what' pathway (Figure 2).
The anterior direction of the processing of intelligible
speech has also been observed using rapid event-related
functional magnetic resonance imaging (fMRI) [28]. In
more anterior fields, rostral to PAC, responses to both
syntactic and semantic violations in sentences can be
seen, implicating this anterior stream in the integration
of lexical information in spoken language [29]. This study
by Friederici et al. [29] also indicated that basal ganglia
regions could be specifically associated with syntactic
processing, evidence that the `language system' as a
whole is associated with regions beyond the temporal
2 Cognitive neuroscience
Figure 1
What
Where
(a)
(b)
Auditory regions and streams in the primate brain. (a) The lateral
surface of a macaque brain showing regions of visual (pink) and
auditory (blue) responsivity (adapted from Poremba et al. [13]).
Multimodal responsivity is shown in purple. (b) Two broad `steams'
of processing within the auditory system (adapted from
Romanski et al. [17]).
Figure 2
What
How
Where
Current Opinion in Neurobiology
(a)
(b)
Functional responses to speech and candidate stream of processing in
the human brain. (a) The lateral surface of the human brain, the coloured
regions indicate broadly to which type of acoustic signal each temporal
region (and associated parietal and frontal region) responds. Regions in
blue show a specific response to language-specific phonological
structure (Jacquemot et al. [27
]). Regions in lilac respond to stimuli with
the phonetic cues and features of speech, whereas those in purple
respond to intelligible speech (Scott et al. [31], Narain et al. [32]). Regions
in pink respond to verbal short term memory and articulatory
representations of speech (Wise et al. [39], Hickok et al. [38], Jacquemot
et al. [27
]). Regions in green respond to auditory spatial tasks (Arnott
et al. [22
]). (b) The putative directions of the `what' `where' and `how'
streams of processing in the human brain.
Current Opinion in Neurobiology 2005, 15:1­5 www.sciencedirect.com

lobes [30]. Further along the anterior stream, in the left
anterior superior temporal sulcus (STS), responses are
seen to intelligible speech [31,32], and this response is
seen for both single words and sentences [33]. Thus, the
anterior `what' system in humans is important in the early
stages of acoustic processing of speech. Responses to
speech can be observed extending into frontal regions;
`top down' modulation of heard speech is associated with
ventral prefrontal [34] and posterior premotor cortex
activation [35
,36]. This suggests a role for frontal audi-
tory connections, and possibly motor representations, in
spoken language processing. Indeed, some research has
suggested that the pattern of responses in auditory cortex
can be highly modulated by task related top-down pro-
cessing [37].
In addition to a clear role for spatial processing of sound in
posterior auditory fields in humans, there is evidence for
at least two further kinds of speech-related auditory
processing in posterior auditory fields, which might or
might not form subsets of the same process. First, it has
been suggested that aspects of verbal working memory
are associated with left posterior STS [38,39] and supra-
marginal gyrus [27
]. This might relate to some of the
issues of the nature of auditory memory -- specifically,
the need for transient representations that encode the
temporal dimension [3]. In addition, medial posterior
fields are activated during speech production [40]
whether or not articulation is overt [39] or even specific
to speech [38]. This implicates posterior auditory cortex
in the guidance of the motor act of speech (and perhaps
other motor acts), and might represent a sensory motor
interface, involved in speech, that links perception and
production. As mentioned in the Introduction, sounds
convey information about the events that cause them, and
a role for motor information has long been posited as a
route for speech perception [41]. These posterior
auditory­motor fields might, therefore, form part of the
same system in which motor cortex [35
] and left anterior
insula [42] responses have been described in functional
imaging studies, and contribute to a `how' system in
speech perception [24,26
,33]. It is also striking that
recordings from caudal medial auditory fields in primates
have shown that they are responsive to touch -- another
potential link for sensory­motor integration [43,44]. The
relationship among this putative `how' pathway, transient
auditory memory systems and the auditory `where'
pathways in humans requires further elaboration; they
might all fall within a system that encodes spatial­motoric
information generically, or they might form distinctly
different subsystems.
Auditory objects, scenes and attention
How do the streams of auditory processing interact with
auditory object processing and auditory scene analysis? It
has been suggested that central auditory mechanisms are
important for paying attention to auditory objects [45].
Single cell recordings from cat PAC have enabled inves-
tigators to identify the plasticity of response in PAC that is
associated with the frequency of auditory objects [46]. In
humans, fMRI has shown that primary auditory cortical
fields are sensitive to the amplitude envelopes of sounds,
and non primary auditory fields also show enhanced
sensitivity to the onsets and offsets of sounds -- phenom-
ena associated with the structure of auditory events [47
].
Evidence also shows that anterior auditory fields are
important for the tracking of auditory streams of informa-
tion [48
]. Moving further from PAC in terms of synaptic
distance, in a PET study Zatorre et al. [49] manipulated
the acoustic cues of auditory objects to create the impres-
sion of multiple events. This revealed activation in right
superior sulcus, anterior to primary auditory cortex, impli-
cating the anterior `what' stream in the representation of
multiple auditory objects. We have also recently shown
that there is extensive processing of an unattended
speaker in lateral and anterior STG, suggesting that
multiple complex auditory objects can be represented
cortically, and thus providing a route for the semantic
processing of `unattended' speech [34]. Therefore, the
`what' stream of processing is apparently also implicated
in the representation of, and perhaps the allocation of
attention to, distinct auditory objects. How this interacts
with posterior `where' stream(s), which has also been
associated with aspects of attention control of the auditory
scene [6] and subcortical nuclei essential for the encoding
of spatial cues, will be developed in further studies.
Returning to our discussion of non-human primates we
look to the work of Poremba et al. [50
], who have been
investigating hemispheric lateralization for the processing
of conspecific vocalizations using PET. They revealed an
anterior superior temporal lobe response to meaningful
vocalizations that was left lateralized. This response is
strikingly similar to that seen to intelligible speech in
human functional imaging studies [31]. Intriguingly, the
asymmetric response was abolished following commissur-
otomy, suggesting that the diminished response to voca-
lizations in the right temporal pole was a result of activity
on the left -- perhaps an active suppression of the right by
the left. Such suppression of the right hemisphere
response has been noted in the right operculum in human
studies of speech production [51]. It has proven difficult
to account for hemispheric asymmetries in linguistic
processing as a result of acoustic properties of the speech
signal [33], although a recent study has suggested that
such asymmetry derives from even simpler differences in
auditory processing [52]. The nature of hemispheric
differences in auditory and linguistic processing will be
illuminated further by the characterization of such hemi-
spheric interactions.
Conclusions
It is not fanciful to suggest that, as the most articulate
primates, we have evolved a neural system optimized for
Auditory processing -- speech, space and auditory objects Scott 3
www.sciencedirect.com Current Opinion in Neurobiology 2005, 15:1­5

aspects of speech perception and production, in contrast
to other specializations (e.g. humans do not use hearing
for hunting). Situating our understanding of speech, space
and auditory objects in the context of the basic neuroa-
natomy of the primate auditory system is a strong position
from which to elaborate on these early perceptual sys-
tems. I am optimistic that future work will develop the
cortical and subcortical basis of the functional organiza-
tion of human and non human hearing. I am also hopeful
that the challenges of hemispheric asymmetries, interac-
tions with attention and perception­production links will
be addressed within a neuroanatomical framework.
Acknowledgements
SK Scott is funded by the Wellcome Trust, SRF GR074414MA. I would
like to thank R Wise and S Rosen for helpful discussions on these topics.
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Auditory processing -- speech, space and auditory objects Scott 5
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