Human temporal lobe activation by speech and nonspeech sounds

Functional organization of the lateral temporal cortex in humans is not well understood. We recorded blood oxygenation signals from the temporal lobes of normal volunteers using functional magnetic resonance imaging during stimulation with unstructured noise, frequency-modulated (FM) tones, reversed speech, pseudowords and words. For all conditions, subjects performed a material-nonspecific detection response when a train of stimuli began or ceased. Dorsal areas surrounding Heschl's gyrus bilaterally, particularly the planum temporale and dorsolateral superior temporal gyrus, were more strongly activated by FM tones than by noise, suggesting a role in processing simple temporally encoded auditory information. Distinct from these dorsolateral areas, regions centered in the superior temporal sulcus bilaterally were more activated by speech stimuli than by FM tones. Identical results were obtained in this region using words, pseudowords and reversed speech, suggesting that the speech-tones activation difference is due to acoustic rather than linguistic factors. In contrast, previous comparisons between word and nonword speech sounds showed left-lateralized activation differences in more ventral temporal and temporoparietal regions that are likely involved in processing lexical-semantic or syntactic information associated with words. The results indicate functional subdivision of the human lateral temporal cortex and provide a preliminary framework for understanding the cortical processing of speech sounds.     

Sound to language: different cortical processing for first and second languages in elementary school children as revealed by a large-scale study using fNIRS

A large-scale study of 484 elementary school children (6-10 years) performing word repetition tasks in their native language (L1-Japanese) and a second language (L2-English) was conducted using functional near-infrared spectroscopy. Three factors presumably associated with cortical activation, language (L1/L2), word frequency (high/low), and hemisphere (left/right), were investigated. L1 words elicited significantly greater brain activation than L2 words, regardless of semantic knowledge, particularly in the superior/middle temporal and inferior parietal regions (angular/supramarginal gyri). The greater L1-elicited activation in these regions suggests that they are phonological loci, reflecting processes tuned to the phonology of the native language, while phonologically unfamiliar L2 words were processed like nonword auditory stimuli. The activation was bilateral in the auditory and superior/middle temporal regions. Hemispheric asymmetry was observed in the inferior frontal region (right dominant), and in the inferior parietal region with interactions: low-frequency words elicited more right-hemispheric activation (particularly in the supramarginal gyrus), while high-frequency words elicited more left-hemispheric activation (particularly in the angular gyrus). The present results reveal the strong involvement of a bilateral language network in children's brains depending more on right-hemispheric processing while acquiring unfamiliar/low-frequency words. A right-to-left shift in laterality should occur in the inferior parietal region, as lexical knowledge increases irrespective of language.     

Spatiotemporal interaction between sound form and meaning during spoken word perception

Cortical dynamics of spoken word perception is not well understood. The possible interplay between analysis of sound form and meaning, in particular, remains elusive. We used magnetoencephalography to study cortical manifestation of phonological and semantic priming. Ten subjects listened to lists of 4 words. The first 3 words set a semantic or phonological context, and the list-final word was congruent or incongruent with this context. Attenuation of activation by priming during the first 3 words and increase of activation to semantic or phonological mismatch in the list-final word provided converging evidence: The superior temporal cortex bilaterally was involved in both analysis of sound form and meaning but the role of each hemisphere varied over time. Sensitivity to sound form was observed at approximately 100 ms after word onset, followed by sensitivity to semantic aspects from approximately 250 ms onwards, in the left hemisphere. From approximately 450 ms onwards, the picture was changed, with semantic effects now present bilaterally, accompanied by a subtle late effect of sound form in the right hemisphere. Present MEG data provide a detailed spatiotemporal account of neural mechanisms during speech perception that may underlie characterizations obtained with other neuroimaging methods less sensitive in temporal or spatial domain.     

Reading salt activates gustatory brain regions: FMRI evidence for semantic grounding in a novel sensory modality

Because many words are typically used in the context of their referent objects and actions, distributed cortical circuits for these words may bind information about their form with perceptual and motor aspects of their meaning. Previous work has demonstrated such semantic grounding for sensorimotor, visual, auditory, and olfactory knowledge linked to words, which is manifest in activation of the corresponding areas of the cortex. Here, we explore the brain basis of gustatory semantic links of words whose meaning is primarily related to taste. In a blocked functional magnetic resonance imaging design, Spanish taste words and control words matched for a range of factors (including valence, arousal, imageability, frequency of use, number of letters and syllables) were presented to 59 right-handed participants in a passive reading task. Whereas all the words activated the left inferior frontal (BA44/45) and the posterior middle and superior temporal gyri (BA21/22), taste-related words produced a significantly stronger activation in these same areas and also in the anterior insula, frontal operculum, lateral orbitofrontal gyrus, and thalamus among others. As these areas comprise primary and secondary gustatory cortices, we conclude that the meaning of taste words is grounded in distributed cortical circuits reaching into areas that process taste sensations.     

Brain mechanisms for reading words and pseudowords: an integrated approach

The present study tested two predictions of dual-process models of reading: (i) that the brain structures involved in sublexical phonological analysis and those involved in whole-word phonological access during reading are different; and (ii) that reading of meaningful items, by means of the addressed phonology process, is mediated by different brain structures than reading of meaningless letter strings. We obtained brain activation profiles using Magnetic Source Imaging and, in addition, pronunciation latencies during reading of: (i) exception words (primarily involving addressed phonology and having meaning), (ii) pseudohomophones (requiring assembled phonology and having meaning), and (iii) pseudowords (requiring assembled phonology but having no meaning). Reading of meaningful items entailed a high degree of activation of the left posterior middle temporal gyrus (MTGp) and mesial temporal lobe areas, whereas reading the meaningless pseudowords was associated with much reduced activation of these two regions. Reading of all three types of print resulted in activation of the posterior superior temporal gyrus (STGp), inferior parietal and basal temporal areas. In addition, pronunciation speed of exception words correlated significantly with the onset of activity in MTGp but not STGp, whereas the opposite was true for pseudohomophones and pseudowords. These findings are consistent with the existence of two different brain mechanisms that support phonological processing in word reading: one mechanism that subserves assembled phonology and depends on the posterior part of STGp, and a second mechanism that is responsible for pronouncing words with rare print-to-sound correspondences and does not necessarily involve this region but instead appears to depend on MTGp.     

Differential sensitivity to words and shapes in ventral occipito-temporal cortex

Efficient extraction of shape information is essential for proficient reading but the role of cortical mechanisms of shape analysis in word reading is not well understood. We studied cortical responses to written words while parametrically varying the amount of visual noise applied to the word stimuli. In only a few regions along the ventral surface, cortical responses increased with word visibility. We found consistently increasing responses in bilateral posterior occipito-temporal sulcus (pOTS), at an anatomical location that closely matches the "visual word form area". In other cortical regions, such as V1, responses remained constant regardless of the noise level. We performed 3 additional tests to assess the functional specialization of pOTS responses for written word processing. We asked whether pOTS responses are 1) left lateralized, 2) more sensitive to words than to line drawings or false fonts, and 3) invariant for visual hemifield of words but not other stimuli. We found that left and right pOTS response functions both had highest sensitivity for words, intermediate for line drawings, and lowest for false fonts. Visual hemifield invariance was similar for words and line drawings. These results suggest that left and right pOTS are both involved in shape processing, with enhanced efficiency for processing visual word forms.     

Dynamics of gamma-band activity induced by auditory pattern changes in humans.

Increasing evidence suggests separate auditory pattern and space processing streams. The present paper describes two magnetoencephalogram studies examining gamma-band activity to changes in auditory patterns using consonant-vowel syllables (experiment 1), animal vocalizations and artificial noises (experiment 2). Two samples of each sound type were presented to passively listening subjects in separate oddball paradigms with 80% standards and 20% deviants differing in their spectral composition. Evoked magnetic mismatch fields peaking approximately 190 ms poststimulus showed a trend for a left-hemisphere advantage for syllables, but no hemispheric differences for the other sounds. Frequency analysis and statistical probability mapping of the differences between deviants and standards revealed increased gamma-band activity above 60 Hz over left anterior temporal/ventrolateral prefrontal cortex for all three types of stimuli. This activity peaked simultaneously with the mismatch responses for animal sounds (180 ms) but was delayed for noises (260 ms) and syllables (320 ms). Our results support the hypothesized role of anterior temporal/ventral prefrontal regions in the processing of auditory pattern change. They extend earlier findings of gamma-band activity over posterior parieto-temporal cortex during auditory spatial processing that supported the putative auditory dorsal stream. Furthermore, earlier gamma-band responses to animal vocalizations may suggest faster processing of fear-relevant information.     

Neural substrates for processing task-irrelevant emotional distracters in maltreated adolescents with depressive disorders: a pilot study

In this pilot study, neural systems related to cognitive and emotional processing were examined using event-related functional magnetic resonance imaging in 5 maltreated youth with depressive disorders and 11 nonmaltreated healthy participants. Subjects underwent an emotional oddball task, where they detected infrequent ovals (targets) within a continual stream of phase-scrambled images (standards). Sad and neutral images were intermittently presented as task-irrelevant distracters. The maltreated youth revealed significantly decreased activation in the left middle frontal gyrus and right precentral gyrus to target stimuli and significantly increased activation to sad stimuli in bilateral amygdala, left subgenual cingulate, left inferior frontal gyrus, and right middle temporal cortex compared to nonmaltreated subjects. Additionally, the maltreated youth showed significantly decreased activation to both attentional targets and sad distracters in the left posterior middle frontal gyrus compared to nonmaltreated subjects. In this exploratory study of dorsal control and ventral emotional circuits, we found that maltreated youth with distress disorders demonstrated dysfunction of neural systems related to cognitive control and emotional processing.     

Functional MRI of sentence comprehension in children with dyslexia: beyond word recognition

Sentence comprehension (SC) studies in typical and impaired readers suggest that reading for meaning involves more extensive brain activation than reading isolated words. Thus far, no reading disability/dyslexia (RD) studies have directly controlled for the word recognition (WR) components of SC tasks, which is central for understanding comprehension processes beyond WR. This experiment compared SC to WR in 29, 9-14 year olds (15 typical and 14 impaired readers). The SC-WR contrast for each group showed activation in left inferior frontal and extrastriate regions, but the RD group showed significantly more activation than Controls in areas associated with linguistic processing (left middle/superior temporal gyri), and attention and response selection (bilateral insula, right cingulate gyrus, right superior frontal gyrus, and right parietal lobe). Further analyses revealed this overactivation was driven by the RD group's response to incongruous sentences. Correlations with out-of-scanner measures showed that better word- and text-level reading fluency was associated with greater left occipitotemporal activation, whereas worse performance on WR, fluency, and comprehension (reading and oral) were associated with greater right hemisphere activation in a variety of areas, including supramarginal and superior temporal gyri. Results provide initial foundations for understanding the neurobiological correlates of higher-level processes associated with reading comprehension.     

Category-specific conceptual processing of color and form in left fronto-temporal cortex

To investigate the cortical basis of color and form concepts, we examined event-related functional magnetic resonance imaging (fMRI) responses to matched words related to abstract color and form information. Silent word reading elicited activity in left temporal and frontal cortex, where category-specific activity differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked category-specific activity in fusiform and middle temporal gyrus as well as premotor and dorsolateral prefrontal areas in inferior and middle frontal gyri. These results demonstrate that word meanings and concepts are not processed by a unique cortical area, but by different sets of areas, each of which may contribute differentially to conceptual semantic processing. We hypothesize that the anterior parahippocampal activation to color words indexes computation of the visual feature conjunctions and disjunctions necessary for classifying visual stimuli under a color concept. The predominant premotor and prefrontal activation to form words suggests action-related information processing and may reflect the involvement of neuronal elements responding in an either-or fashion to mirror neurons related to adumbrating shapes.     

The functional neuroanatomy of metrical stress evaluation of perceived and imagined spoken words

We hypothesized that areas in the temporal lobe that have been implicated in the phonological processing of spoken words would also be activated during the generation and phonological processing of imagined speech. We tested this hypothesis using functional magnetic resonance imaging during a behaviorally controlled task of metrical stress evaluation. Subjects were presented with bisyllabic words and had to determine the alternation of strong and weak syllables. Thus, they were required to discriminate between weak-initial words and strong-initial words. In one condition, the stimuli were presented auditorily to the subjects (by headphones). In the other condition the stimuli were presented visually on a screen and subjects were asked to imagine hearing the word. Results showed activation of the supplementary motor area, inferior frontal gyrus (Broca's area) and insula in both conditions. In the superior temporal gyrus (STG) and in the superior temporal sulcus (STS) strong activation was observed during the auditory (perceptual) condition. However, a region located in the posterior part of the STS/STG also responded during the imagery condition. No activation of this same region of the STS was observed during a control condition which also involved processing of visually presented words, but which required a semantic decision from the subject. We suggest that processing of metrical stress, with or without auditory input, relies in part on cortical interface systems located in the posterior part of STS/STG. These results corroborate behavioral evidence regarding phonological loop involvement in auditory-verbal imagery.     

The role of semantics and grammatical class in the neural representation of words

On the basis of neuropsychological and functional imaging evidence, meaning and grammatical class (particularly the verb-noun distinction) have been proposed as organizational principles of linguistic knowledge in the brain. However, previous studies investigating verb and noun processing have been confounded by the presence of systematic correlations between word meaning and grammatical class. In this positron emission tomography study, we investigated implicit word processing using stimuli that allowed the effects of semantic and grammatical properties to be examined independently, without grammatical-semantic confounds. We found that left hemisphere cortical activation during single-word processing was modulated by word meaning, but not by grammatical class. Motor word processing produced significant activation in left precentral gyrus, whereas sensory word processing produced significant activation in left inferior temporal and inferior frontal regions. In contrast to previous studies, there were no effects of grammatical class in left inferior frontal gyrus (IFG). Instead, we found semantic-based differences within left IFG: anterior, but not posterior, left IFG regions responded preferentially to sensory words. These findings demonstrate that the neural substrates of implicit word processing are determined by semantic rather than grammatical properties and suggest that word comprehension involves the activation of modality-specific representations linked to word meaning.     

Spatiotemporal signatures of large-scale synfire chains for speech processing as revealed by MEG

We report a new brain signature of memory trace activation in the human brain revealed by magnetoencephalography and distributed source localization. Spatiotemporal patterns of cortical activation can be picked up in the time course of source images underlying magnetic brain responses to speech and noise stimuli, especially the generators of the magnetic mismatch negativity. We found that acoustic signals perceived as speech elicited a well-defined spatiotemporal pattern of sequential activation of superior-temporal and inferior-frontal cortex, whereas the same identical stimuli, when perceived as noise, did not elicit temporally structured activation. Strength of local sources constituting large-scale spatiotemporal patterns reflected additional lexical and syntactic features of speech. Morphological processing of the critical sound as verb inflection led to particularly pronounced early left inferior-frontal activation, whereas the same sound functioning as inflectional affix of a noun activated superior-temporal cortex more strongly. We conclude that precisely timed spatiotemporal patterns involving specific cortical areas may represent a brain code of memory circuit activation. These spatiotemporal patterns are best explained in terms of synfire mechanisms linking neuronal populations in different cortical areas. The large-scale synfire chains appear to reflect the processing of stimuli together with the context-dependent perceptual and cognitive information bound to them.     

PET Activation of Posterior Temporal Regions during Auditory Word Presentation and Verb Generation

Previous studies using positron emission tomography (PET) reportblood flow changes in superior and middle temple gyri associatedwith auditory and language tasks (Petersen et al., 1988, 1989;Wise et al., 1991; Demonet et al., 1992; Howard et al., 1992Sergent et al., 1992; Zatorre et al., 1992; Petrides et al.,1993; Raichle et al., 1994; Fiez et al., 1995). An importantissue is whether these changes reflect the activation of a singlefunctional region or multiple regions with distinct functionalcontributions. In the present study, we examined this issueby focusing upon two tasks for which we have previously reportedposterior temporal blood flow changes: listening to auditorilypresented words (Petersen et al., 1988, 1989), and generationof a verb in response to a visually presented noun (Raichleet al., 1994); see also Wise et al. (1991). We began by furthercharacterizing a left temporoparietal region of change previouslyassociated with auditory word presentation. This previouslyreported response was replicated, and the results were extendedby demonstrating presentation of pseudowords also produced activation.We next asked whether the activation associated with auditoryword presentation could be distinguished from that associatedwith the generation of verbs in response to visually presentednouns. It was found that the activations associated with thesetwo tasks could be both functionally and spatially dissociated.Thus, two posterior temporal areas associated with auditoryword presentation and verb generation appear to represent distinctareas concerned with word processing. More generally, the resultsdemonstrate an approach for assessing the independence of twoactivated areas.     

Conjoint and extended neural networks for the computation of speech codes: the neural basis of selective impairment in reading words and pseudowords

The computation of speech codes (i.e. phonology) is an important aspect of word reading. Understanding the neural systems and mech- anisms underlying phonological processes provides a foundation for the investigation of language in the brain. We used high-resolution three-dimensional positron emission tomography (PET) to investigate neural systems essential for phonological processes. The burden of neural activities on the computation of speech codes was maximized by three rhyming tasks (rhyming words, pseudowords and words printed in mixed letter cases). Brain activation patterns associated with these tasks were compared with those of two baseline tasks involving visual feature detection. Results suggest strong left lateralized epicenters of neural activity in rhyming irrespective of gender. Word rhyming activated the same brain regions engaged in pseudoword rhyming, suggesting conjoint neural networks for phonological processing of words and pseudowords. However, pseudoword rhyming induced the largest change in cerebral blood flow and activated more voxels in the left posterior prefrontal regions and the left inferior occipital-temporal junction. In addition, pseudoword rhyming activated the left supramarginal gyrus, which was not apparent in word rhyming. These results suggest that rhyming pseudowords requires active participation of extended neural systems and networks not observed for rhyming words. The implications of the results on theories and models of visual word reading and on selective reading dysfunctions after brain lesions are discussed.     

Neural interactions at the core of phonological and semantic priming of written words

Word processing is often probed with experiments where a target word is primed by preceding semantically or phonologically related words. Behaviorally, priming results in faster reaction times, interpreted as increased efficiency of cognitive processing. At the neural level, priming reduces the level of neural activation, but the actual neural mechanisms that could account for the increased efficiency have remained unclear. We examined whether enhanced information transfer among functionally relevant brain areas could provide such a mechanism. Neural activity was tracked with magnetoencephalography while subjects read lists of semantically or phonologically related words. Increased priming resulted in reduced cortical activation. In contrast, coherence between brain regions was simultaneously enhanced. Furthermore, while the reduced level of activation was detected in the same area and time window (superior temporal cortex [STC] at 250-650 ms) for both phonological and semantic priming, the spatiospectral connectivity patterns appeared distinct for the 2 processes. Causal interactions further indicated a driving role for the left STC in phonological processing. Our results highlight coherence as a neural mechanism of priming and dissociate semantic and phonological processing via their distinct connectivity profiles.     

Brain activation for consonants and vowels

Previous behavioral and electrophysiological studies have shown dissociation between consonants and vowels. We used functional magnetic resonance imaging to investigate whether vowel and consonant processing differences are expressed in the neuronal activation pattern and whether they are modulated by task. The experimental design involved reading aloud and lexical decision on visually presented pseudowords created by transposing or replacing consonants or vowels in words. During reading aloud, changing vowels relative to consonants increased activation in a right middle temporal area previously associated with prosodic processing of speech input. In contrast, during lexical decision, changing consonants relative to vowels increased activation in a right middle frontal area associated with inhibiting go-responses. The task-sensitive nature of these effects demonstrates that consonants and vowels differ at a processing, rather than stimulus, level. We argue that prosodic processing of vowel changes arise during self-monitoring of speech output, whereas greater inhibition of go-responses to consonant changes follows insufficient lexico-semantic processing when nonwords looking particularly like words must be rejected. Our results are consistent with claims that vowels and consonants place differential demands on prosodic and lexico-semantic processing, respectively. They also highlight the different types of information that can be drawn from functional imaging and neuropsychological studies.     

Cortical representation of sign language: comparison of deaf signers and hearing non-signers

Numerous studies have demonstrated activation of the classical left-hemisphere language areas when native signers process sign language. More recently, specific sign language-related processing has been suggested to occur in homologous areas of the right hemisphere as well. We now show that these cortical areas are also activated in hearing non-signers during passive viewing of signs that for them are linguistically meaningless. Neuromagnetic activity was stronger in deaf signers than in hearing non-signers in the region of the right superior temporal sulcus and the left dorsal premotor cortex, probably reflecting familiarity and linguistic meaningfulness of the observed movement sequences. In contrast, the right superior parietal lobule, the mesial parieto-occipital region, and the mesial paracentral lobule were more strongly activated in hearing non-signers, apparently reflecting active visuomotor encoding of complex unfamiliar movement sequences.     

Segregating semantic and syntactic aspects of processing in the human brain: an fMRI investigation of different word types

The processing of single words that varied in their semantic (concrete/abstract word) and syntactic (content/function word) status was investigated under different task demands (semantic/ syntactic task) in an event-related functional magnetic resonance imaging experiment. Task demands to a large degree determined which subparts of the neuronal network supporting word processing were activated. Semantic task demands selectively activated the left pars triangularis of the inferior frontal gyrus (BA 45) and the posterior part of the left middle/superior temporal gyrus (BA 21/22/37). In contrast, syntactic processing requirements led to an increased activation in the inferior tip of the left frontal operculum (BA 44) and the cortex lining the junction of the inferior frontal and inferior precentral sulcus (BA 44/6). Moreover, for these latter areas a word class by concreteness interaction was observed when a syntactic judgement was required. This interaction can be interpreted as a prototypicality effect: non-prototypical members of a word class, i.e. concrete function words and abstract content words, showed a larger activation than prototypical members, i.e. abstract function words and concrete content words. The combined data suggest that the activation pattern underlying word processing is predicted neither by syntactic class nor semantic concreteness but, rather, by task demands focusing either on semantic or syntactic aspects. Thus, our findings that semantic and syntactic aspects of processing are both functionally distinct and involve different subparts of the neuronal network underlying word processing support a domain-specific organization of the language system.     

Cortical processing of complex auditory stimuli during alterations of consciousness with the general anesthetic propofol

BACKGROUND: The extent to which complex auditory stimuli are processed and differentiated during general anesthesia is unknown. The authors used blood oxygenation level-dependent functional magnetic resonance imaging to examine the processing words (10 per period; compared with scrambled words) and nonspeech human vocal sounds (10 per period; compared with environmental sounds) during propofol anesthesia. METHODS: Seven healthy subjects were tested. Propofol was given by a computer-controlled pump to obtain stable plasma concentrations. Data were acquired during awake baseline, sedation (propofol concentration in arterial plasma: 0.64 +/- 0.13 microg/ml; mean +/- SD), general anesthesia (4.62 +/- 0.57 microg/ml), and recovery. Subjects were asked to memorize the words. RESULTS: During all periods including anesthesia, the sounds conditions combined elicited significantly greater activations than silence bilaterally in primary auditory cortices (Heschl gyrus) and adjacent regions within the planum temporale. During sedation and anesthesia, however, the magnitude of the activations was reduced by 40-50% (P < 0.05). Furthermore, anesthesia abolished voice-specific activations seen bilaterally in the superior temporal sulcus during the other periods as well as word-specific activations bilaterally in the Heschl gyrus, planum temporale, and superior temporal gyrus. However, scrambled words paradoxically elicited significantly more activation than normal words bilaterally in planum temporale during anesthesia. Recognition the next day occurred only for words presented during baseline plus recovery and was correlated (P < 0.01) with activity in right and left planum temporale. CONCLUSIONS: The authors conclude that during anesthesia, the primary and association auditory cortices remain responsive to complex auditory stimuli, but in a nonspecific way such that the ability for higher-level analysis is lost.