Phonological processing in human auditory cortical fields

David L Woods, Timothy J Herron, Anthony D Cate, Xiaojian Kang, E W Yund, David L Woods, Timothy J Herron, Anthony D Cate, Xiaojian Kang, E W Yund

Abstract

We used population-based cortical-surface analysis of functional magnetic imaging data to characterize the processing of consonant-vowel-consonant syllables (CVCs) and spectrally matched amplitude-modulated noise bursts (AMNBs) in human auditory cortex as subjects attended to auditory or visual stimuli in an intermodal selective attention paradigm. Average auditory cortical field (ACF) locations were defined using tonotopic mapping in a previous study. Activations in auditory cortex were defined by two stimulus-preference gradients: (1) Medial belt ACFs preferred AMNBs and lateral belt and parabelt fields preferred CVCs. This preference extended into core ACFs with medial regions of primary auditory cortex (A1) and the rostral field preferring AMNBs and lateral regions preferring CVCs. (2) Anterior ACFs showed smaller activations but more clearly defined stimulus preferences than did posterior ACFs. Stimulus preference gradients were unaffected by auditory attention suggesting that ACF preferences reflect the automatic processing of different spectrotemporal sound features.

Keywords: asymmetry; auditory cortex; consonant; fMRI; phonemes; primary auditory cortex; selective attention; speech.

Figures

Figure 1
Figure 1
(A) Cortical surface locations of activation peaks associated with the phonological processing of speech sounds as reported in the metanalysis of Turkeltaub and Coslett (2010). Talairach coordinates were projected onto the average cortical surface of 60 subjects using VAMCA (nitrc.org/projects/vamca). Gray = gyri, black = sulci. Dots show the cortical surface locations of the reported Talairach coordinates on each of the hemispheres of 60 individual subjects (red = left, blue = right) that were used to estimate the median location. Cyan crosses show the median location of activations in the left hemisphere, yellow crosses show the median location of activations in the right hemisphere. The results were superimposed on the average cortical surface boundaries of functionally defined auditory cortical fields from Woods et al. (2010b). (B) Cortical surface locations of the regions that responded most strongly to consonant–vowel (CV) syllables in comparison with bird song elements, sounds of musical instruments, or animal sounds, from Leaver and Rauschecker (2010). HG, Heschl's Gyrus; STG, superior temporal gyrus; STS, superior temporal sulcus; MTG, middle temporal gyrus. Core ACFs: A1, primary auditory cortex; R, rostral field; RT, rostrotemporal field. Medial belt ACFs: CM, caudomedial field; RM, rostromedial field; RTM, rostrotemporal medial field. Lateral belt ACFs: CL, caudolateral field; ML, mid-lateral field; AL, anterior–lateral field; RTL, rostrotemporal lateral field. Parabelt ACFs: CPB, caudal parabelt field; RPB, rostral parabelt field.
Figure 2
Figure 2
Intermodal selective attention block design. Stimuli were presented in blocks lasting 29.6 s. In speech conditions, subjects discriminated triads of consonant–vowel–consonant (CVC) syllables. Within each block, two consonants (one voiced, one unvoiced) were used that shared place (front, middle, or back) and manner of articulation (plosive or fricative). Consonants were combined with 3 different vowels to create 12 different CVC syllables. Recordings of the 12 CVCs were obtained twice from each of four different talkers to create 96 different tokens that were sampled randomly. Subjects focused attention on the modality cued by a letter at fixation (e.g., “A” = auditory, top) and performed a one-back, triad matching task. During attend-CVC conditions, subjects matched CVC triads regardless of talker. In non-speech conditions, subjects discriminated the frequency-modulation pattern of triads of syllable-length amplitude modulated noise bursts (AMNBs). AMNBs were amplitude modulated at four different frequencies. Different AMNBs were spectrally matched to each of the four talkers. During visual attention conditions subjects discriminated triads of open, closed, or exploded rectangles. On bimodal blocks, auditory and visual stimuli were presented asynchronously to minimize multimodal integration. Attend-auditory (red) and attend-visual (blue) blocks occurred in constrained random order. Block conditions: UV, unimodal visual; UA, unimodal auditory; BV, bimodal, visual attention; BA, bimodal auditory. Enlarged: BA block with front plosives (/p/ and /b/). Talker: female talker 1, female talker 2, male talker 1, male talker 2. Target = asterisk.
Figure 3
Figure 3
Cortical surface analysis. The cortex from each subject was segmented with FreeSurfer (Fischl et al., 1999b) then inflated to a sphere and aligned to a common coordinate system. The functional and anatomical data were then mapped onto a Mollweide equal-area projection after rotating the sphere so that the intersection of Heschls gyrus (HG) and the superior temporal gyrus (STG) lay at map center with the STG aligned along the equator. Stimulus-dependent activations (SDAs) averaged over all auditory stimulation conditions and subjects are shown on the average anatomy of the left hemisphere. Activations were restricted to the regions of auditory cortex near HG with the outlined region enlarged in the figures shown below. Colored voxels show voxels showing highly significant activations (t > 7.0) with mean percent signal changes ranging from 0.1 to 0.6% (red to yellow).
Figure 4
Figure 4
Quantifying activations. (A) Mean percent signal change (0.05–0.58%) of activations coded by brightness. Color shows stimulus preferences (red = CVC, green = AMNB). Yellow areas were activated by both stimulus classes. See text for ACF labels. (B) ACF locations projected on average curvature map of the superior temporal plane (green = gyri, red = sulci), showing anatomical structures and grids used for quantification. Green = gyri, red = sulci. CiS, circular sulcus; HG, Heschl's gyrus; HS, Heschl's sulcus; PT, planum temporale; STG, superior temporal gyrus; STS, superior temporal sulcus, LGI, long gyri of the insula.
Figure 5
Figure 5
Stimulus preferences of different field groups showing mean activation magnitudes and the percent enhancement within each field group for CVC syllables vs. amplitude modulated speech-spectrum noise bursts (AMNB).
Figure 6
Figure 6
Attentional modulation of different field groups showing activation magnitudes and mean percentage of attentional enhancement for each field group. UA = unimodal auditory, BA = bimodal auditory attention, BV = bimodal visual attention.
Figure 7
Figure 7
Normalized timecourses of SDAs and ARMs in different ACF groups. Auditory stimulus delivery ceased at approximately 28.5s, but attention effects persisted into the next stimulus block.
Figure 8
Figure 8
Tuning preferences of grid elements in A1 from medial to lateral boundaries along approximate isofrequency contours estimated using tonotopic maps from Woods et al. (2010c). Low = 125–500 Hz, Mid = 500–2000 Hz, High = 2000–8000 Hz.
Figure 9
Figure 9
Tuning preferences of grid elements in R from medial to lateral boundaries along approximate isofrequency contours estimated from tonotopic maps from Woods et al. (2010c). See Figure 8 for frequency values.
Figure 10
Figure 10
A schematic map of ACFs showing stimulus preferences (red = CVC, green = SSNB) with the R/G color mixture reflecting the relative magnitude of activations to the two stimulus categories. Significant differences in tuning properties of adjacent fields are indicated. S = CVC stimulus preference, C = contralaterality, A = attentional modulation, H = right/left hemispheric asymmetry. For example, primary auditory cortex (A1) showed significantly greater contralaterality, but reduced speech-preference, attentional modulation, and relative right-hemisphere amplitudes in comparison with the adjacent lateral belt field, ML. Tonotopic extrema of A1 and R: h = high frequency responsive area, L = low frequency responsive area.

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