Einat Liebenthal

Neural correlates of sensory and decision processes in auditory object identification.

Physiological studies of auditory perception have not yet clearly distinguished sensory from decision processes. In this experiment, human participants identified speech sounds masked by varying levels of noise while blood oxygenation signals in the brain were recorded with functional magnetic resonance imaging (fMRI). Accuracy and response time were used to characterize the behavior of sensory and decision components of this perceptual system. Oxygenation signals in a cortical subregion just anterior and lateral to primary auditory cortex predicted accuracy of sound identification, whereas signals in an inferior frontal region predicted response time. Our findings provide neurophysiological evidence for a functional distinction between sensory and decision mechanisms underlying auditory object identification. The present results also indicate a link between inferior frontal lobe activation and response-selection processes during auditory perception tasks.

Syntactic and Semantic Modulation of Neural Activity during Auditory Sentence Comprehension

In previous functional neuroimaging studies, left anterior temporal and temporal-parietal areas responded more strongly to sentences than to randomly ordered lists of words. The smaller response for word lists could be explained by either (1) less activation of syntactic processes due to the absence of syntactic structure in the random word lists or (2) less activation of semantic processes resulting from failure to combine the content words into a global meaning. To test these two explanations, we conducted a functional magnetic resonance imaging study in which word order and combinatorial word meaning were independently manipulated during auditory comprehension. Subjects heard six different stimuli: normal sentences, semantically incongruent sentences in which content words were randomly replaced with other content words, pseudoword sentences, and versions of these three sentence types in which word order was randomized to remove syntactic structure. Effects of syntactic structure (greater activation to sentences than to word lists) were observed in the left anterior superior temporal sulcus and left angular gyrus. Semantic effects (greater activation to semantically congruent stimuli than either incongruent or pseudoword stimuli) were seen in widespread, bilateral temporal lobe areas and the angular gyrus. Of the two regions that responded to syntactic structure, the angular gyrus showed a greater response to semantic structure, suggesting that reduced activation for word lists in this area is related to a disruption in semantic processing. The anterior temporal lobe, on the other hand, was relatively insensitive to manipulations of semantic structure, suggesting that syntactic information plays a greater role in driving activation in this area.

Tonotopic organization of human auditory cortex

The organization of tonotopic fields in human auditory cortex was investigated using functional magnetic resonance imaging. Subjects were presented with stochastically alternating multi-tone sequences in six different frequency bands, centered at 200, 400, 800, 1600, 3200, and 6400 Hz. Two mirror-symmetric frequency gradients were found extending along an anterior-posterior axis from a zone on the lateral aspect of Heschls gyrus (HG), which responds preferentially to lower frequencies, toward zones posterior and anterior to HG that are sensitive to higher frequencies. The orientation of these two principal gradients is thus roughly perpendicular to HG, rather than parallel as previously assumed. A third, smaller gradient was observed in the lateral posterior aspect of the superior temporal gyrus. The results suggest close homologies between the tonotopic organization of human and nonhuman primate auditory cortex.

Simultaneous ERP and fMRI of the auditory cortex in a passive oddball paradigm.

Infrequent occurrences of a deviant sound within a sequence of repetitive standard sounds elicit the automatic mismatch negativity (MMN) event-related potential (ERP). The main MMN generators are located in the superior temporal cortex, but their number, precise location, and temporal sequence of activation remain unclear. In this study, ERP and functional magnetic resonance imaging (fMRI) data were obtained simultaneously during a passive frequency oddball paradigm. There were three conditions, a STANDARD, a SMALL deviant, and a LARGE deviant. A clustered image acquisition technique was applied to prevent contamination of the fMRI data by the acoustic noise of the scanner and to limit contamination of the electroencephalogram (EEG) by the gradient-switching artifact. The ERP data were used to identify areas in which the blood oxygenation (BOLD) signal varied with the magnitude of the negativity in each condition. A significant ERP MMN was obtained, with larger peaks to LARGE deviants and with frontocentral scalp distribution, consistent with the MMN reported outside the magnetic field. This result validates the experimental procedures for simultaneous ERP/fMRI of the auditory cortex. Main foci of increased BOLD signal were observed in the right superior temporal gyrus [STG; Brodmann area (BA) 22] and right superior temporal plane (STP; BA 41 and 42). The imaging results provide new information supporting the idea that generators in the right lateral aspect of the STG are implicated in processes of frequency deviant detection, in addition to generators in the right and left STP.

Time course of semantic processes during sentence comprehension: an fMRI study.

The ability to create new meanings from combinations of words is one important function of the language system. We investigated the neural correlates of combinatorial semantic processing using fMRI. During scanning, participants performed a rating task on auditory word or pseudoword strings that differed in the presence of combinatorial and word-level semantic information. Stimuli included normal sentences comprised of thematically related words that could be readily combined to produce a more complex meaning, semantically incongruent sentences in which content words were randomly replaced with other content words, pseudoword sentences, and versions of these three sentence types in which syntactic structure was removed by randomly re-ordering the words. Several regions showed greater BOLD signal for stimuli with words than for those with pseudowords, including the left angular gyrus, left superior temporal sulcus, and left inferior frontal gyrus, suggesting that these areas are involved in semantic access at the single word level. In the angular and inferior frontal gyri these differences emerged early in the course of the hemodynamic response. An effect of combinatorial semantic structure was observed in the left angular gyrus and left lateral temporal lobe, which showed greater activation for normal compared to semantically incongruent sentences. These effects appeared later in the time course of the hemodynamic response, beginning after the entire stimulus had been presented. The data indicate a complex spatiotemporal pattern of activity associated with computation of word and sentence-level semantic information, and suggest a particular role for the left angular gyrus in processing overall sentence meaning.

Volumetric vs. surface-based alignment for localization of auditory cortex activation.

The high degree of intersubject structural variability in the human brain is an obstacle in combining data across subjects in functional neuroimaging experiments. A common method for aligning individual data is normalization into standard 3D stereotaxic space. Since the inherent geometry of the cortex is that of a 2D sheet, higher precision can potentially be achieved if the intersubject alignment is based on landmarks in this 2D space. To examine the potential advantage of surface-based alignment for localization of auditory cortex activation, and to obtain high-resolution maps of areas activated by speech sounds, fMRI data were analyzed from the left hemisphere of subjects tested with phoneme and tone discrimination tasks. We compared Talairach stereotaxic normalization with two surface-based methods: Landmark Based Warping, in which landmarks in the auditory cortex were chosen manually, and Automated Spherical Warping, in which hemispheres were aligned automatically based on spherical representations of individual and average brains. Examination of group maps generated with these alignment methods revealed superiority of the surface-based alignment in providing precise localization of functional foci and in avoiding mis-registration due to intersubject anatomical variability. Human left hemisphere cortical areas engaged in complex auditory perception appear to lie on the superior temporal gyrus, the dorsal bank of the superior temporal sulcus, and the lateral third of Heschls gyrus.

Specialization along the Left Superior Temporal Sulcus for Auditory Categorization

The affinity and temporal course of functional fields in middle and posterior superior temporal cortex for the categorization of complex sounds was examined using functional magnetic resonance imaging (fMRI) and event-related potentials (ERPs) recorded simultaneously. Data were compared before and after subjects were trained to categorize a continuum of unfamiliar nonphonemic auditory patterns with speech-like properties (NP) and a continuum of familiar phonemic patterns (P). fMRI activation for NP increased after training in left posterior superior temporal sulcus (pSTS). The ERP P2 response to NP also increased with training, and its scalp topography was consistent with left posterior superior temporal generators. In contrast, the left middle superior temporal sulcus (mSTS) showed fMRI activation only for P, and this response was not affected by training. The P2 response to P was also independent of training, and its estimated source was more anterior in left superior temporal cortex. Results are consistent with a role for left pSTS in short-term representation of relevant sound features that provide the basis for identifying newly acquired sound categories. Categorization of highly familiar phonemic patterns is mediated by long-term representations in left mSTS. Results provide new insight regarding the function of ventral and dorsal auditory streams.

Left posterior temporal regions are sensitive to auditory categorization

Recent studies suggest that the left superior temporal gyrus and sulcus (LSTG/S) play a role in speech perception, although the precise function of these areas remains unclear. Here, we test the hypothesis that regions in the LSTG/S play a role in the categorization of speech phonemes, irrespective of the acoustic properties of the sounds and prior experience of the listener with them. We examined changes in functional magnetic resonance imaging brain activation related to a perceptual shift from nonphonetic to phonetic analysis of sine-wave speech analogs. Subjects performed an identification task before scanning and a discrimination task during scanning with phonetic (P) and nonphonetic (N) sine-wave sounds, both before (Pre) and after (Post) being exposed to the phonetic properties of the P sounds. Behaviorally, experience with the P sounds induced categorical identification of these sounds. In the PostP > PreP and PostP > PostN contrasts, an area in the posterior LSTG/S was activated. For both P and N sounds, the activation in this region was correlated with the degree of categorical identification in individual subjects. The results suggest that these areas in the posterior LSTG/S are sensitive neither to the acoustic properties of speech nor merely to the presence of phonetic information, but rather to the listeners awareness of category representations for auditory inputs.

Attentional and linguistic interactions in speech perception.

The role of attention in speech comprehension is not well understood. We used fMRI to study the neural correlates of auditory word, pseudoword, and nonspeech (spectrally rotated speech) perception during a bimodal (auditory, visual) selective attention task. In three conditions, Attend Auditory (ignore visual), Ignore Auditory (attend visual), and Visual (no auditory stimulation), 28 subjects performed a one-back matching task in the assigned attended modality. The visual task, attending to rapidly presented Japanese characters, was designed to be highly demanding in order to prevent attention to the simultaneously presented auditory stimuli. Regardless of stimulus type, attention to the auditory channel enhanced activation by the auditory stimuli (Attend Auditory>Ignore Auditory) in bilateral posterior superior temporal regions and left inferior frontal cortex. Across attentional conditions, there were main effects of speech processing (word+pseudoword>rotated speech) in left orbitofrontal cortex and several posterior right hemisphere regions, though these areas also showed strong interactions with attention (larger speech effects in the Attend Auditory than in the Ignore Auditory condition) and no significant speech effects in the Ignore Auditory condition. Several other regions, including the postcentral gyri, left supramarginal gyrus, and temporal lobes bilaterally, showed similar interactions due to the presence of speech effects only in the Attend Auditory condition. Main effects of lexicality (word>pseudoword) were isolated to a small region of the left lateral prefrontal cortex. Examination of this region showed significant word>pseudoword activation only in the Attend Auditory condition. Several other brain regions, including left ventromedial frontal lobe, left dorsal prefrontal cortex, and left middle temporal gyrus, showed Attention x Lexicality interactions due to the presence of lexical activation only in the Attend Auditory condition. These results support a model in which neutral speech presented in an unattended sensory channel undergoes relatively little processing beyond the early perceptual level. Specifically, processing of phonetic and lexical-semantic information appears to be very limited in such circumstances, consistent with prior behavioral studies.

Attentional Modulation in the Detection of Irrelevant Deviance: A Simultaneous ERP/fMRI Study

Little is known about the neural mechanisms that control attentional modulation of deviance detection in the auditory modality. In this study, we manipulated the difficulty of a primary task to test the relation between task difficulty and the detection of infrequent, task-irrelevant deviant (D) tones (1300 Hz) presented among repetitive standard (S) tones (1000 Hz). Simultaneous functional magnetic resonance imaging (fMRI)/event-related potentials (ERPs) were recorded from 21 subjects performing a two-alternative forced-choice duration discrimination task (short and long tones of equal probability). The duration of the short tone was always 50 msec. The duration of the long tone was 100 msec in the easy task and 60 msec in the difficult task. As expected, response accuracy decreased and response time (RT) increased in the difficult compared with the easy task. Performance was also poorer for D than for S tones, indicating distraction by task-irrelevant frequency information on trials involving D tones. In the difficult task, an amplitude increase was observed in the difference waves for N1 and P3a, ERP components associated with increased attention to deviant sounds. The mismatch negativity (MMN) response, associated with passive deviant detection, was larger in the easy task, demonstrating the susceptibility of this component to attentional manipulations. The fMRI contrast D > S in the difficult task revealed activation on the right superior temporal gyrus (STG) and extending ventrally into the superior temporal sulcus, suggesting this regions involvement in involuntary attention shifting toward unattended, infrequent sounds. Conversely, passive deviance detection, as reflected by the MMN, was associated with more dorsal activation on the STG. These results are consistent with the view that the dorsal STG region is responsive to mismatches between the memory trace of the standard and the incoming deviant sound, whereas the ventral STG region is activated by involuntary shifts of attention to task-irrelevant auditory features.