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Functional maps of human auditory cortex: effects of acoustic features and attention.

Woods DL, Stecker GC, Rinne T, Herron TJ, Cate AD, Yund EW, Liao I, Kang X - PLoS ONE (2009)

Bottom Line: Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks.The results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes.Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

View Article: PubMed Central - PubMed

Affiliation: Human Cognitive Neurophysiology Laboratory, VANCHCS, Martinez, California, United States of America. dlwoods@ucdavis.edu

ABSTRACT

Background: While human auditory cortex is known to contain tonotopically organized auditory cortical fields (ACFs), little is known about how processing in these fields is modulated by other acoustic features or by attention.

Methodology/principal findings: We used functional magnetic resonance imaging (fMRI) and population-based cortical surface analysis to characterize the tonotopic organization of human auditory cortex and analyze the influence of tone intensity, ear of delivery, scanner background noise, and intermodal selective attention on auditory cortex activations. Medial auditory cortex surrounding Heschl's gyrus showed large sensory (unattended) activations with two mirror-symmetric tonotopic fields similar to those observed in non-human primates. Sensory responses in medial regions had symmetrical distributions with respect to the left and right hemispheres, were enlarged for tones of increased intensity, and were enhanced when sparse image acquisition reduced scanner acoustic noise. Spatial distribution analysis suggested that changes in tone intensity shifted activation within isofrequency bands. Activations to monaural tones were enhanced over the hemisphere contralateral to stimulation, where they produced activations similar to those produced by binaural sounds. Lateral regions of auditory cortex showed small sensory responses that were larger in the right than left hemisphere, lacked tonotopic organization, and were uninfluenced by acoustic parameters. Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks. Attention-related modulations (ARMs) were larger in lateral than medial regions of auditory cortex and appeared to arise primarily in belt and parabelt auditory fields. ARMs lacked tonotopic organization, were unaffected by acoustic parameters, and had distributions that were distinct from those of sensory responses. Unlike the gradual adaptation seen for sensory responses, ARMs increased in amplitude throughout stimulus blocks.

Conclusions/significance: The results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes. Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

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A schematic model of human auditory cortical fields.Schematic representations of primate auditory cortical fields (Kaas & Hackett, 2000) superimposed on frequency-specific activation patterns in human auditory cortex. Field borders were estimated based on similarities in tonotopic organization observed in the current study and in fMRI studies of macaque auditory cortex (Petkov et al. 2006, Kayser et al. 2007). Colors show frequency tuning of grand mean activations averaged over subjects, hemispheres, image acquisition parameters, tone location and tone intensity. Red = 3600 Hz, green = 900 Hz, blue = 225 Hz. A1 = primary auditory cortex; R = rostral, T = temporal, M = middle; A = Anterior; L = lateral, C = caudal, PB = parabelt.
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pone-0005183-g014: A schematic model of human auditory cortical fields.Schematic representations of primate auditory cortical fields (Kaas & Hackett, 2000) superimposed on frequency-specific activation patterns in human auditory cortex. Field borders were estimated based on similarities in tonotopic organization observed in the current study and in fMRI studies of macaque auditory cortex (Petkov et al. 2006, Kayser et al. 2007). Colors show frequency tuning of grand mean activations averaged over subjects, hemispheres, image acquisition parameters, tone location and tone intensity. Red = 3600 Hz, green = 900 Hz, blue = 225 Hz. A1 = primary auditory cortex; R = rostral, T = temporal, M = middle; A = Anterior; L = lateral, C = caudal, PB = parabelt.

Mentions: Anatomical and functional studies of auditory cortex in the macaque have revealed thirteen different ACFs [56]. Figure 14 shows a schematic model of these fields superimposed on the grand mean tonotopic maps from the current study using a model similar to models of macaque auditory cortex [13], [57]. The model assumes that frequency-selective activations occur primarily at borders between ACFs that share common frequency tuning. For example, the H1 region is hypothesized to reflect combined activations in the high-frequency region of A1 as well as high-frequency regions in four surrounding mirror-symmetric belt fields. Similarly, L1 would reflect activations in the anterior region of A1 that is responsive to low frequencies as well as activations in surrounding low-frequency regions in R and lateral belt fields ML and AL. Thus, the principal tonotopic axis connecting fields H1-L1-H2 would include activations in core and belt regions. However, in comparison with existing maps of macaque auditory cortex, activations in human auditory cortex reveal more extensive activations in non-tonotopic regions that are lateral and posterior to the tonotopic representations. These non-tonotopic activations likely arise in caudal regions of auditory cortex that are equivalent to parabelt fields and that include Tpt [58], a region that may have undergone expansion in humans relative to other primate species [59].


Functional maps of human auditory cortex: effects of acoustic features and attention.

Woods DL, Stecker GC, Rinne T, Herron TJ, Cate AD, Yund EW, Liao I, Kang X - PLoS ONE (2009)

A schematic model of human auditory cortical fields.Schematic representations of primate auditory cortical fields (Kaas & Hackett, 2000) superimposed on frequency-specific activation patterns in human auditory cortex. Field borders were estimated based on similarities in tonotopic organization observed in the current study and in fMRI studies of macaque auditory cortex (Petkov et al. 2006, Kayser et al. 2007). Colors show frequency tuning of grand mean activations averaged over subjects, hemispheres, image acquisition parameters, tone location and tone intensity. Red = 3600 Hz, green = 900 Hz, blue = 225 Hz. A1 = primary auditory cortex; R = rostral, T = temporal, M = middle; A = Anterior; L = lateral, C = caudal, PB = parabelt.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2664477&req=5

pone-0005183-g014: A schematic model of human auditory cortical fields.Schematic representations of primate auditory cortical fields (Kaas & Hackett, 2000) superimposed on frequency-specific activation patterns in human auditory cortex. Field borders were estimated based on similarities in tonotopic organization observed in the current study and in fMRI studies of macaque auditory cortex (Petkov et al. 2006, Kayser et al. 2007). Colors show frequency tuning of grand mean activations averaged over subjects, hemispheres, image acquisition parameters, tone location and tone intensity. Red = 3600 Hz, green = 900 Hz, blue = 225 Hz. A1 = primary auditory cortex; R = rostral, T = temporal, M = middle; A = Anterior; L = lateral, C = caudal, PB = parabelt.
Mentions: Anatomical and functional studies of auditory cortex in the macaque have revealed thirteen different ACFs [56]. Figure 14 shows a schematic model of these fields superimposed on the grand mean tonotopic maps from the current study using a model similar to models of macaque auditory cortex [13], [57]. The model assumes that frequency-selective activations occur primarily at borders between ACFs that share common frequency tuning. For example, the H1 region is hypothesized to reflect combined activations in the high-frequency region of A1 as well as high-frequency regions in four surrounding mirror-symmetric belt fields. Similarly, L1 would reflect activations in the anterior region of A1 that is responsive to low frequencies as well as activations in surrounding low-frequency regions in R and lateral belt fields ML and AL. Thus, the principal tonotopic axis connecting fields H1-L1-H2 would include activations in core and belt regions. However, in comparison with existing maps of macaque auditory cortex, activations in human auditory cortex reveal more extensive activations in non-tonotopic regions that are lateral and posterior to the tonotopic representations. These non-tonotopic activations likely arise in caudal regions of auditory cortex that are equivalent to parabelt fields and that include Tpt [58], a region that may have undergone expansion in humans relative to other primate species [59].

Bottom Line: Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks.The results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes.Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

View Article: PubMed Central - PubMed

Affiliation: Human Cognitive Neurophysiology Laboratory, VANCHCS, Martinez, California, United States of America. dlwoods@ucdavis.edu

ABSTRACT

Background: While human auditory cortex is known to contain tonotopically organized auditory cortical fields (ACFs), little is known about how processing in these fields is modulated by other acoustic features or by attention.

Methodology/principal findings: We used functional magnetic resonance imaging (fMRI) and population-based cortical surface analysis to characterize the tonotopic organization of human auditory cortex and analyze the influence of tone intensity, ear of delivery, scanner background noise, and intermodal selective attention on auditory cortex activations. Medial auditory cortex surrounding Heschl's gyrus showed large sensory (unattended) activations with two mirror-symmetric tonotopic fields similar to those observed in non-human primates. Sensory responses in medial regions had symmetrical distributions with respect to the left and right hemispheres, were enlarged for tones of increased intensity, and were enhanced when sparse image acquisition reduced scanner acoustic noise. Spatial distribution analysis suggested that changes in tone intensity shifted activation within isofrequency bands. Activations to monaural tones were enhanced over the hemisphere contralateral to stimulation, where they produced activations similar to those produced by binaural sounds. Lateral regions of auditory cortex showed small sensory responses that were larger in the right than left hemisphere, lacked tonotopic organization, and were uninfluenced by acoustic parameters. Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks. Attention-related modulations (ARMs) were larger in lateral than medial regions of auditory cortex and appeared to arise primarily in belt and parabelt auditory fields. ARMs lacked tonotopic organization, were unaffected by acoustic parameters, and had distributions that were distinct from those of sensory responses. Unlike the gradual adaptation seen for sensory responses, ARMs increased in amplitude throughout stimulus blocks.

Conclusions/significance: The results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes. Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

Show MeSH
Related in: MedlinePlus