Task-modulated "what" and "where" pathways in human auditory cortex

Abstract

Human neuroimaging studies suggest that localization and identification of relevant auditory objects are accomplished via parallel parietal-to-lateral-prefrontal "where" and anterior-temporal-to-inferior-frontal "what" pathways, respectively. Using combined hemodynamic (functional MRI) and electromagnetic (magnetoencephalography) measurements, we investigated whether such dual pathways exist already in the human nonprimary auditory cortex, as suggested by animal models, and whether selective attention facilitates sound localization and identification by modulating these pathways in a feature-specific fashion. We found a double dissociation in response adaptation to sound pairs with phonetic vs. spatial sound changes, demonstrating that the human nonprimary auditory cortex indeed processes speech-sound identity and location in parallel anterior "what" (in anterolateral Heschl's gyrus, anterior superior temporal gyrus, and posterior planum polare) and posterior "where" (in planum temporale and posterior superior temporal gyrus) pathways as early as approximately 70-150 ms from stimulus onset. Our data further show that the "where" pathway is activated approximately 30 ms earlier than the "what" pathway, possibly enabling the brain to use top-down spatial information in auditory object perception. Notably, selectively attending to phonetic content modulated response adaptation in the "what" pathway, whereas attending to sound location produced analogous effects in the "where" pathway. This finding suggests that selective-attention effects are feature-specific in the human nonprimary auditory cortex and that they arise from enhanced tuning of receptive fields of task-relevant neuronal populations.

Fig. 1.

Schematic illustration of the experimental paradigm and phenomenon of neuronal adaptation. (a) Sound stimuli. Pairs of Finnish vowels/æ/and/ø/were presented from straight ahead or 45° to the right. (b) Sound sequence and tasks. Vowel pairs (i.e., Adaptor followed by Probe) were spatially discordant, phonetically discordant, or identical. During consecutive blocks, subjects were instructed to attend to either spatial (Attend Location) or phonetic (Attend Phoneme) similarities between successive sound pairs or to ignore the presented stimuli (Ignore condition not shown here). In the Attend Location condition, the subject responded to sound pairs that matched the spatial pattern of the preceding sound pair (same directions in same order), irrespective of the phonetic content. In the Attend Phoneme condition, the targets were, in turn, sound pairs being phonetically similar to the preceding sound pair (same phonemes in same order), irrespective of the spatial content. (c) Schematic illustration of response adaptation. A Probe sound preceded by an identical Adaptor produces a strongly adapted response. Adaptation is weakest when Probe differs from Adaptor in a feature to which the neuronal population is sharply tuned.

Fig. 2.

Differential adaptation to phonemes vs. sound locations in nonprimary auditory cortex. Cortical fMRI-weighted MEG source estimates are shown in a representative subject at the N1 peak latency. The auditory cortex areas activated by the Adaptor (the first stimulus of the pair) are identical across the conditions, but specific adaptation-induced differences in activity patterns elicited by Probes (the second stimulus of the pair) are observed: The posterior activity is strongest (i.e., least adapted) when Adaptor and Probe differ spatially, and the anterior activity is strongest when Adaptor and Probe differ phonetically. The results were similar in the right hemisphere of this subject (not shown here). STS, superior temporal sulcus.

Fig. 3.

ROI analysis of fMRI-weighted MEG source estimates to Probe sounds, showing differential adaptation after location vs. phoneme changes in the posterior and anterior auditory cortex, respectively. (a) The ROI locations in a representative subject are represented on the inflated cortex. (b) The ROI group average results suggest sharper spatial tuning in the posterior and sharper phoneme tuning in the anterior auditory cortex regions. The statistical significances refer to a priori Helmert contrast between the condition of interest (Location Change in the posterior and Phoneme Change in the anterior ROI) vs. other conditions.

Fig. 4.

Group-average ECD results of the two N1 subcomponents (50, 52, 53) showing the attentional modulation of the anterior and posterior auditory cortex activity to Probes following spatially or phonetically different Adaptors. The ECD locations (Top), group-averaged in a spherical standard space (60), are displayed on the inflated brain hemispheres of one subject. (Middle and Bottom) The source waveforms were amplitude-normalized within each subject before calculating the group averages (shown as Z-score values). This procedure retains the within-subject amplitude proportions, and each subject contributes equally to the group mean. Insets demonstrate the responses at −50–400 ms around Probes from sources showing peak attention effects. The N1 response amplitudes to Probes (encircled) are modulated task-dependently. The posterior N1 activity to Probes following spatially different Adaptors is enhanced by spatial attention. The anterior N1 activity to Probes following phonetically different Adaptors is enhanced by phonetic attention.

Fig. 5.

Group-average selective attention effects in the right (Upper) and left (Lower) auditory cortices in ECD estimates. The response amplitudes to Probes are modulated task-dependently: The posterior N1 activity is enhanced by spatial attention, and the anterior N1 activity is enhanced by phonetic attention. The figure also shows the differential adaptation in the anterior and posterior N1 sources for phonetic vs. spatial information, respectively.