Download Functional imaging of human auditory cortex

Functional imaging of human auditory cortex
David L. Woodsa,b,c,d and Claude Alaine,f
a
Human Cognitive Neurophysiology Laboratory,
VANCHCS, Martinez, bDepartment of Neurology, UC
Davis, cCenter for Neurosciences, UC Davis, dCenter
for Mind and Brain, UC Davis, Davis, California, USA,
e
Rotman Research Institute, Baycrest Centre and
f
Department of Psychology, University of Toronto,
Toronto, Canada
Correspondence to Dr David L. Woods, Neurology
Service (127E), VANCHCS, 150 Muir Road, Martinez,
CA 95553, USA
Tel: +1 925 372 2571; fax: +1 925 229 2315;
e-mail: [email protected]
Current Opinion in Otolaryngology & Head and
Neck Surgery 2009, 17:407–411
Purpose of review
This review summarizes recent advances in functional magnetic resonance imaging that
reveal similarities in the organization of human auditory cortex (HAC) and auditory cortex
of nonhuman primates.
Recent findings
Functional magnetic resonance imaging studies have shown that HAC is a compact
region that covers less than 8% of the total cortical surface. HAC is subdivided into
more than a dozen distinct auditory cortical fields (ACFs) that surround Heschl’s gyri on
the superior temporal plane. Recent advances that permit the visualization of the results
of functional magnetic imaging experiments directly on the cortical surface have
provided new insights into the organization of human ACFs. Evidence suggests that
medial regions of HAC are organized in a manner similar to the auditory cortex of other
primate species with a set of tonotopically organized core ACFs surrounded by belt
ACFs that often share tonotopic organization with the core. Although influenced by
attention, responses in HAC core and belt fields are largely determined by the acoustic
properties of stimuli, including their frequency, intensity, and location. In contrast, lateral
regions of HAC contain parabelt fields that are little influenced by simple acoustic
features but rather respond to behaviorally relevant complex sounds such as speech
and are strongly modulated by attention.
Summary
HAC conserves the basic structural and functional organization of auditory cortex as
seen in old world primate species. A central challenge to future research is to
understand how this basic primate plan has evolved to support uniquely human abilities
such as music and language.
Keywords
attention, auditory cortex, auditory cortical fields, plasticity, tonotopy
Curr Opin Otolaryngol Head Neck Surg 17:407–411
ß 2009 Wolters Kluwer Health | Lippincott Williams & Wilkins
1068-9508
Introduction
Recent advances in functional neuroimaging have made
it possible to visualize the cortical regions that are activated during sensory perception. Apparently unitary
perceptual experience actually involves the parallel
activation of many different sensory representations
on the cortical surface. For example, visually responsive
regions cover more than 30% of the cortical surface and
are divided into more than 30 distinct visual cortical
fields that analyze different attributes of visual stimuli
[1] including complex biologically significant signals such
as faces [2].
Primate auditory cortex is also thought to contain more
than a dozen auditory cortical fields (ACFs) as shown in
Fig. 1a [3]. Central regions of auditory cortex are divided
into core fields that receive direct projections from the
ventral nucleus of the medial geniculate body and have
the cellular characteristics of primary sensory cortex and
surrounding belt fields that receive projections from the
1068-9508 ß 2009 Wolters Kluwer Health | Lippincott Williams & Wilkins
dorsal medial geniculate body and have cytoarchitectonic
characteristics of association cortex [3,4].
Some progress has been made in understanding the role
that different ACFs play in the analysis of auditory
signals. However, auditory cortex is small (occupying less
than 8% of the total cortical surface) and includes a
number of fields that are largely inaccessible to neurophysiological recordings because of their locations within
the Sylvian fissure. Roughly half of the ACFs so far
studied show some evidence of tonotopic organization
[5]. Functional magnetic resonance imaging (fMRI)
studies of humans have revealed an organizational plan
that is similar to that found in other primate species as
summarized in the current review.
Locating human auditory cortex
Recent advances in neuroimaging technology [6] have
made it possible to create average anatomical maps from
populations of human participants that preserve the
DOI:10.1097/MOO.0b013e3283303330
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
408 Hearing science
Figure 1 A representation of primate auditory cortex
centered slightly posteriorly to the tip of anterior Heschl’s
gyrus and extending posterior-medially in Heschl’s sulcus
and onto the superior temporal plane (Fig. 1d).
Tonotopic organization
(a) Twelve auditory cortical fields (ACFs) in the macaque with tonotopic
fields colored to show frequency organization (red indicates high, blue
indicates low). Core regions (A1, R, and RT) show mirror-symmetric
tonotopic organization. See [3] for further details. (b) Average cortical
curvature pattern of 60 participants. Green indicates gyri, red indicates
sulci. The entire hemisphere is displayed using a Mollweide equal-area
projection with auditory cortex at the center. (c) Population-averaged
activations produced by broadband acoustic stimuli (speech sounds
and speech-spectrum noise bursts) during visual attention when sounds
were unattended. Activations are restricted to auditory cortex surrounding HG and the STG. The rectangular region shows the area enlarged in
subpart (d) and in Fig. 2 below. (d) Meta-analysis of cortical-surface
locations of Te1.1 (equivalent to A1) identified in postmortem cytoarchitectonic studies. Yellow indicates cortical-surface locations seen in
more than 50% of participants. The rectangle shows region highlighted
in subpart c. See text for further details. HG, Heschl’s gyrus; STG,
superior temporal gyrus.
detailed patterns of cortical folding and curvature to
permit the accurate visualization of gyral structures,
including Heschl’s gyrus, at the center of auditory cortex
(Fig. 1b). fMRI activations can be coregistered with
these anatomical maps to permit the cortical activations
elicited by unattended sounds to be precisely localized
on the cortical surface. These studies reveal that auditory
cortex occupies 50–80 cm2 of the cortical surface
surrounding Heschl’s gyrus (Fig. 1c). Human auditory
cortex (HAC) extends anterior–posteriorly from the
planum polare to the planum temporale and medial–
laterally from insular regions slightly medial to the tip of
Heschl’s gyrus to the lateral surface of the superior
temporal gyrus (STG).
Primary auditory cortex is characterized by its granular
cytoarchitecture that has been mapped in the human brain
using combined postmortem imaging and histological
studies [7–10]. When the three-dimensional stereotaxic
coordinates of A1 described in these histological studies
are projected onto an average cortical curvature map using
cortical-surface meta-analysis tools (http://www.ebire.org/
hcnlab), A1 has a relatively consistent anatomical location
in relation to surrounding gyral structures: A1 is typically
Anatomical and functional studies of primates have
suggested that auditory cortex contains a number of
ACFs that are divided into central core fields and surrounding belt and parabelt fields as shown in Fig. 1a [11].
Many ACFs are organized tonotopically, that is, with a
frequency representation mapped onto the cortical surface. In particular, the core fields at the center of auditory
cortex have a mirror-symmetric tonotopic organization.
Primary auditory cortex (A1) has a high-to-low frequency
representation that abuts with a mirror-imaged representation (i.e., low-to-high) in the rostral core field (R). In
addition, many of the belt fields also show tonotopic
organization that often parallels that of the adjacent core
field [12]. The mirror-symmetric tonotopic organization
has been verified in fMRI studies of macaques [13].
A number of studies have examined the tonotopic organization of human auditory cortex [14–22] with results
that vary somewhat based on stimulus and scanning
parameters. However, when the distributions reported
in these studies are subjected to meta-analysis and the
results projected onto average cortical-surface anatomy, a
relatively consistent tonotopic organization emerges
(Fig. 2a). High-frequency sounds activate a small lateral
region anterior to the intersection of Heschl’s gyrus and
the STG and a more extensive medial region posterior
to the tip of Heschl’s gyrus. In contrast, low-frequency
sounds activate lateral regions centered on mid-Heschl’s
gyrus and extending posteriorly along the STG.
The details of tonotopic organization can be more precisely visualized when activations are analyzed directly
to the cortical surface of individual participants [19,20].
For example, Formisano et al. [23] found clear evidence
of mirror-symmetric tonotopy when activations to tones
of different frequency were mapped to the cortex of
individual participants. Details of single-participant cortical-surface maps may be influenced by idiosyncrasies
in the venous anatomy of individual participants [24],
but population-averaged cortical-surface analysis reveals
a similar pattern, as shown in Fig. 2b [25]. Highfrequency tones (red) produce two foci of activation:
a prominent band of activation posterior to Heschl’s
gyrus (H1) and a smaller patch of activation anterior to
Heschl’s gyrus near its border with the STG (H2). Lowfrequency tones (blue) produce a consistent activation in
mid-Heschl’s gyrus (L1) and inconsistent activations
in more lateral fields (L-Lat). Finally, intermediatefrequency tones activate intervening regions (M1 and
M2) along the H1–L1–H2 axis. In contrast, lateral
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Functional imaging of human auditory cortex Woods and Alain 409
Figure 2 A representation of tonotopic organization
(a) Meta-analysis of 10 fMRI studies (see text) of frequency tuning in human auditory cortex showing cortical-surface regions responsive to high
frequencies (red) and low frequencies (blue). HG, Heschl’s gyrus (anterior). (b) Average mirror-symmetric tontopic organization from data analyzed
directly using cortical-surface techniques. Regions H1 and H2 are tuned to high frequencies, region L1 is tuned to low frequencies. Intermediate
regions M1 and M2 are tuned to mid-frequencies. Adapted from [25]. , 3600 Hz; , 900 Hz; , 225 Hz. (c) Meta-analysis of 26 studies showing
mean cortical-surface locations of activations in studies in which frequencies varied (freq, red) vs. studies in which locations varied (locat, blue). From
Alho et al. (in preparation). (d) Contrasting distributions of activations associated with increases in sound intensity (green) and selective attention (red).
Yellow zones were sensitive to both increased intensity and attention. Adapted from [25]. (e) Speech-sensitive regions of auditory cortex identified by
contrasting activations to spoken syllables with activations to speech-spectrum noise bursts matched to syllables in frequency, intensity and duration.
Red/yellow indicate increased activation to syllables, blue/cyan indicate increased activation to noise bursts. Contrasts were obtained during
conditions in which participants performed a difficult visual task and sounds were unattended. , Attn; , Intensity; , Both. (f) A schematic model of
human auditory cortical fields (ACFs) based on primate studies and superimposed on the observed human tonotopic map. Frequency-specific
activations are most prominent at boundaries between mirror-symmetric tonotopic fields. Medial regions are sensitive to the acoustic features of
sounds (e.g., frequency, intensity, location), whereas lateral regions process more complex stimuli such as speech and are strongly modulated by
attention.
parabelt regions of auditory cortex show a general
preference for low and middle frequencies but no consistent tonotopic organization that is evident in population-averaged analyses.
Processing other acoustic features
Activations in central regions of auditory cortex surrounding Heschl’s gyrus are strongly influenced by the acoustic
parameters of sounds. For example, increasing the intensity of sounds results in systematic increases in the amplitude of activations in central regions of auditory cortex
[21,25,26–29]. Moreover, the spatial distribution of activations changes with changes in sound intensity, consistent with an ampliotopic organization [25,30]. Activations
in auditory cortex are also influenced by sound location:
activations in each hemisphere are substantially larger to
sounds delivered to the contralateral than to the ipsilateral
ear [22,31], whereas binaural sounds elicit activations that
are similar to those produced by contralateral monaural
sounds [25,32].
In addition, changes in sound features elicit activations
that can reveal the tuning properties of different regions
of auditory cortex. Primate studies show that neurons in
posterior ACFs appear to be more sharply tuned to the
sound location than more anterior ACFs [5] whereas
neurons in anterior ACFs are more sharply tuned to
spectral features [33]. Figure 2c shows the results of
the meta-analysis of 26 studies comparing the activation
foci associated with the detection of infrequent pitch
changes (red crosses) with the activation foci associated
with infrequent changes in the sound location (blue
crosses). The average location of activations to pitch
changes was significantly anterior to the activation
foci to location changes, consistent with suggestions of
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
410 Hearing science
distinct auditory ‘what’ and ‘where’ auditory pathways in
HAC [34–36].
in surrounding belt and parabelt regions. These lateral
regions lack tonotopic organization, are tuned to more
complex and behaviorally relevant sounds such as speech
and are strongly modulated by attention.
Complex stimuli: vocalizations
Neurophysiological studies suggest that anterior belt
fields in macaques are preferentially engaged in the
analysis of primate vocalizations [33], and Petkov et al.
[37] recently used fMRI to identify a vocalizationspecific area in the anterior parabelt fields. Its location
was similar to that of vocalization-specific regions previously identified in human fMRI studies [38,39].
Figure 2d shows speech-specific activations in the human
parabelt vocalization area (PVA) isolated in conditions
in which participants were performing a difficult visual
task. Speech-specific enhancements in activations were
restricted to the PVA, whereas activations in tonotopically organized central ACFs were slightly larger to the
speech spectrum noise bursts. These results suggest that
in humans, as in macaques, there is an anterior PVA that is
specialized to process conspecific vocalizations.
The critical role of auditory attention
Although auditory attention is difficult to investigate in
nonhuman primates, human studies demonstrate that
attention has a powerful influence on auditory processing
in many regions of HAC [40–47]. Intermodal selective
attention studies [22,25,44,48,49] reveal that the largest
attentional modulations are seen in lateral regions
of auditory cortex. Interestingly, attention does not
simply amplify sensory activations in a manner similar
to increasing sound intensity. Rather, attention enhances
activations in nontonotopic lateral regions of auditory
cortex, whereas increasing sound intensity enhances
activations in central ACFs as shown in Fig. 2e.
References and recommended reading
Papers of particular interest, published within the annual period of review, have
been highlighted as:
of special interest
of outstanding interest
Additional references related to this topic can also be found in the Current
World Literature section in this issue (p. 416).
1
Orban GA, Van Essen D, Vanduffel W. Comparative mapping of higher visual
areas in monkeys and humans. Trends Cogn Sci 2004; 8:315–324.
2
Pinsk MA, Arcaro M, Weiner KS, et al. Neural representations of faces and
body parts in macaque and human cortex: a comparative FMRI study. J
Neurophysiol 2009; 101:2581–2600.
3
Kaas JH, Hackett TA, Tramo MJ. Auditory processing in primate cerebral
cortex. Curr Opin Neurobiol 1999; 9:164–170.
4
Pandya DN. Anatomy of the auditory cortex. Rev Neurol 1995; 151:486–494.
5
Recanzone GH, Sutter ML. The biological basis of audition. Annu Rev Psychol
2008; 59:119–142.
6
Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis II: Inflation
flattening and a surface-based coordinate system. Neuroimage 1999;
9:195–207.
7
Morosan P, Rademacher J, Schleicher A, et al. Human primary auditory cortex:
cytoarchitectonic subdivisions and mapping into a spatial reference system.
Neuroimage 2001; 13:684–701.
8
Rademacher J, Morosan P, Schormann T, et al. Probabilistic mapping and
volume measurement of human primary auditory cortex. Neuroimage 2001;
13:669–683.
9
Eickhoff SB, Stephan KE, Mohlberg H, et al. A new SPM toolbox for
combining probabilistic cytoarchitectonic maps and functional imaging data.
Neuroimage 2005; 25:1325–1335.
10 Eickhoff SB, Paus T, Caspers S, et al. Assignment of functional activations to
probabilistic cytoarchitectonic areas revisited. Neuroimage 2007; 36:511–
521.
11 Kaas JH, Hackett TA. Subdivisions of auditory cortex and processing streams
in primates. Proc Natl Acad Sci U S A 2000; 97:11793–11799.
12 Hackett TA, Preuss TM, Kaas JH. Architectonic identification of the core
region in auditory cortex of macaques, chimpanzees, and humans. J Comp
Neurol 2001; 441:197–222.
13 Petkov CI, Kayser C, Augath M, et al. Functional imaging reveals numerous
fields in the monkey auditory cortex. PLoS Biol 2006; 4:e215.
Conclusion
Brain imaging studies have revealed that HAC shares a
pattern of functional organization with nonhuman primate
species. These similarities are reflected in a schematic
model of HAC shown in Fig. 2f. Central regions of
HAC show a tonotopic organization similar to that seen
in other primate species. Frequency-specific fMRI activations likely reflect activations at the boundaries of ACFs
where several adjacent fields share similar frequency
tuning.
Activations in central core and belt areas are largely
determined by basic acoustic features, including intensity, spectral content and sound location. Anterior regions
preferentially analyze spectro-temporal content whereas
posterior regions preferentially analyze sound location.
Although activations in core regions of auditory cortex
can be modulated by attention, attention effects increase
14 Bilecen D, Scheffler K, Schmid N, et al. Tonotopic organization of the
human auditory cortex as detected by BOLD-FMRI. Hear Res 1998;
126:19–27.
15 Engelien A, Yang Y, Engelien W, et al. Physiological mapping of human
auditory cortices with a silent event-related fMRI technique. Neuroimage
2002; 16:944–953.
16 Schonwiesner M, von Cramon DY, Rubsamen R. Is it tonotopy after all?
Neuroimage 2002; 17:1144–1161.
17 Upadhyay J, Ducros M, Knaus TA, et al. Function and connectivity in human
primary auditory cortex: a combined fMRI and DTI study at 3 Tesla. Cereb
Cortex 2007; 17:2420–2432.
18 Wessinger CM, Buonocore MH, Kussmaul CL, et al. Tonotopy in human
auditory cortex examined with functional magnetic resonance imaging. Human
Brain Mapp 1997; 5:18–25.
19 Talavage TM, Sereno MI, Melcher JR, et al. Tonotopic organization in human
auditory cortex revealed by progressions of frequency sensitivity. J Neurophysiol 2004; 91:1282–1296.
20 Talavage TM, Ledden PJ, Benson RR, et al. Frequency-dependent responses
exhibited by multiple regions in human auditory cortex. Hear Res 2000;
150:225–244.
21 Scarff CJ, Dort JC, Eggermont JJ, et al. The effect of MR scanner noise on
auditory cortex activity using fMRI. Hum Brain Mapp 2004; 22:341–349.
22 Petkov CI, Kang X, Alho K, et al. Attentional modulation of human auditory
cortex. Nat Neurosci 2004; 7:658–663.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Functional imaging of human auditory cortex Woods and Alain 411
23 Formisano E, Kim DS, Di Salle F, et al. Mirror-symmetric tonotopic maps in
human primary auditory cortex. Neuron 2003; 40:859–869.
24 Hall DA, Goncalves MS, Smith S, et al. A method for determining venous
contribution to BOLD contrast sensory activation. Magn Reson Imaging
2002; 20:695–706.
25 Woods DL, Stecker GC, Rinne T, et al. Functional maps of human auditory
cortex: effects of acoustic features and attention. PLoS ONE 2009; 4:e5183.
A population-based cortical-surface analysis of tonotopic organization of human
auditory cortex. Also investigates the effects of sound intensity, sound location, and
selective attention on activations in auditory cortex.
26 Jancke L, Shah NJ, Posse S, et al. Intensity coding of auditory stimuli: an fMRI
study. Neuropsychologia 1998; 36:875–883.
27 Langers DR, van Dijk P, Schoenmaker ES, et al. fMRI activation in relation to
sound intensity and loudness. Neuroimage 2007; 35:709–718.
28 Lasota KJ, Ulmer JL, Firszt JB, et al. Intensity-dependent activation of the
primary auditory cortex in functional magnetic resonance imaging. J Comp
Assist Tomogr 2003; 27:213–218.
29 Brechmann A, Baumgart F, Scheich H. Sound-level-dependent representation of frequency modulations in human auditory cortex: a low-noise fMRI
study. J Neurophysiol 2002; 87:423–433.
37 Petkov CI, Kayser C, Steudel T, et al. A voice region in the monkey brain. Nat
Neurosci 2008; 11:367–374.
The above shows the identification of a voice-sensitive parabelt region in
macaques.
38 Belin P, Zatorre RJ, Lafaille P, et al. Voice-selective areas in human auditory
cortex. Nature 2000; 403:309–312.
39 Obleser J, Boecker H, Drzezga A, et al. Vowel sound extraction in anterior
superior temporal cortex. Hum Brain Mapp 2006; 27:562–571.
40 Lipschutz B, Kolinsky R, Damhaut P, et al. Attention-dependent changes of
activation and connectivity in dichotic listening. Neuroimage 2002; 17:643–
656.
41 Alho K, Medvedev SV, Pakhomov SV, et al. Selective tuning of the left and
right auditory cortices during spatially directed attention. Brain Research.
Cogn Brain Res 1999; 7:335–341.
42 Tzourio N, Massioui FE, Crivello L, et al. Functional anatomy of human auditory
attention studied with PET. Neuroimage 1997; 5:63–77.
43 Jancke L, Buchanan TW, Lutz K, et al. Focused and nonfocused attention in
verbal and emotional dichotic listening: an FMRI study. Brain Lang 2001;
78:349–363.
30 Bilecen D, Seifritz E, Scheffler K, et al. Amplitopicity of the human auditory
cortex: an fMRI study. Neuroimage 2002; 17:710–718.
44 Ciaramitaro VM, Buracas GT, Boynton GM. Spatial and cross-modal attention
alter responses to unattended sensory information in early visual and auditory
human cortex. J Neurophysiol 2007; 98:2399–2413.
31 Behne N, Scheich H, Brechmann A. Contralateral white noise selectively
changes right human auditory cortex activity caused by a FM-direction task.
J Neurophysiol 2005; 93:414–423.
45 Rinne T, Balk MH, Koistinen S, et al. Auditory selective attention modulates
activation of human inferior colliculus. J Neurophysiol 2008; 100:3323–
3327.
32 Jancke L, Wustenberg T, Schulze K, et al. Asymmetric hemodynamic responses of the human auditory cortex to monaural and binaural stimulation.
Hear Res 2002; 170:166–178.
46 Krumbholz K, Eickhoff SB, Fink GR. Feature- and object-based attentional
modulation in the human auditory ‘where’ pathway. J Cogn Neurosci 2007;
19:1721–1733.
33 Tian B, Reser D, Durham A, et al. Functional specialization in rhesus monkey
auditory cortex. Science 2001; 292:290–293.
47 Hall DA, Haggard MP, Akeroyd MA, et al. Modulation and task effects in
auditory processing measured using fMRI. Hum Brain Mapp 2000; 10:107–
119.
34 Rauschecker JP, Tian B. Mechanisms and streams for processing of ‘what’ and
‘where’ in auditory cortex. Proc Natl Acad Sci U S A 2000; 97:11800–11806.
35 Arnott SR, Binns MA, Grady CL, et al. Assessing the auditory dual-pathway
model in humans. Neuroimage 2004; 22:401–408.
48 Woodruff PW, Benson RR, Bandettini PA, et al. Modulation of auditory and
visual cortex by selective attention is modality-dependent. Neuroreport 1996;
7:1909–1913.
36 Alain C, Arnott SR, Hevenor S, et al. ‘What’ and ‘where’ in the human auditory
system. Proc Natl Acad Sci U S A 2001; 98:12301–12306.
49 Sabri M, Binder JR, Desai R, et al. Attentional and linguistic interactions in
speech perception. Neuroimage 2008; 39:1444–1456.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.