Decreased connectivity between the thalamus and the neocortex during human nonrapid eye movement sleep.

STUDY OBJECTIVES: To determine whether thalamocortical signaling between the thalamus and the neocortex decreases from wakefulness to nonrapid eye movement (NREM) sleep. DESIGN: Electroencephalography and functional magnetic resonance imaging data were collected simultaneously at 02:30 after 44 h of sleep deprivation. SETTING: Clinical research hospital. PARTICIPANTS: There were six volunteers (mean age 24.2 y, one male) who yielded sufficient amounts of usable, artifact-free data. All were healthy, right-handed native English speakers who consumed less than 710 mL of caffeinated beverages per day. Psychiatric, neurological, circadian, and sleep disorders were ruled out by reviewing each patient's clinical history. A standard clinical nocturnal polysomnogram was negative for sleep disorders. INTERVENTIONS: N/A. MEASUREMENTS AND RESULTS: A functional connectivity analysis was performed using the centromedian nucleus as the seed region. We determined the statistical significance of the difference between correlations obtained during wakefulness and during slow wave sleep. Neocortical regions displaying decreased thalamic connectivity were all heteromodal regions (e.g., medial frontal gyrus and posterior cingulate/precuneus), whereas there was a complete absence of neocortical regions displaying increased thalamic connectivity. Although more clusters of significant decreases were observed in stage 2 sleep, these results were similar to the results for slow wave sleep. CONCLUSIONS: Results of this study provide evidence of a functional deafferentation of the neocortex during nonrapid eye movement (NREM) sleep in humans. This deafferentation likely accounts for increased sensory awareness thresholds during NREM sleep. Decreased thalamocortical connectivity in regions such as the posterior cingulate/precuneus also are observed in coma and general anesthesia, suggesting that changes in thalamocortical connectivity may act as a universal "control switch" for changes in consciousness that are observed in coma, general anesthesia, and natural sleep.

Rhythmic alternating patterns of brain activity distinguish rapid eye movement sleep from other states of consciousness.

Rapid eye movement (REM) sleep constitutes a distinct "third state" of consciousness, during which levels of brain activity are commensurate with wakefulness, but conscious awareness is radically transformed. To characterize the temporal and spatial features of this paradoxical state, we examined functional interactions between brain regions using fMRI resting-state connectivity methods. Supporting the view that the functional integrity of the default mode network (DMN) reflects "level of consciousness," we observed functional uncoupling of the DMN during deep sleep and recoupling during REM sleep (similar to wakefulness). However, unlike either deep sleep or wakefulness, REM was characterized by a more widespread, temporally dynamic interaction between two major brain systems: unimodal sensorimotor areas and the higher-order association cortices (including the DMN), which normally regulate their activity. During REM, these two systems become anticorrelated and fluctuate rhythmically, in reciprocally alternating multisecond epochs with a frequency ranging from 0.1 to 0.01 Hz. This unique spatiotemporal pattern suggests a model for REM sleep that may be consistent with its role in dream formation and memory consolidation.

Auditory cortical activity during cochlear implant-mediated perception of spoken language, melody, and rhythm.

Despite the significant advances in language perception for cochlear implant (CI) recipients, music perception continues to be a major challenge for implant-mediated listening. Our understanding of the neural mechanisms that underlie successful implant listening remains limited. To our knowledge, this study represents the first neuroimaging investigation of music perception in CI users, with the hypothesis that CI subjects would demonstrate greater auditory cortical activation than normal hearing controls. H(2) (15)O positron emission tomography (PET) was used here to assess auditory cortical activation patterns in ten postlingually deafened CI patients and ten normal hearing control subjects. Subjects were presented with language, melody, and rhythm tasks during scanning. Our results show significant auditory cortical activation in implant subjects in comparison to control subjects for language, melody, and rhythm. The greatest activity in CI users compared to controls was seen for language tasks, which is thought to reflect both implant and neural specializations for language processing. For musical stimuli, PET scanning revealed significantly greater activation during rhythm perception in CI subjects (compared to control subjects), and the least activation during melody perception, which was the most difficult task for CI users. These results may suggest a possible relationship between auditory performance and degree of auditory cortical activation in implant recipients that deserves further study.

Neural aspects of sentence comprehension: syntactic complexity, reversibility, and reanalysis.

Broca's area is preferentially activated by reversible sentences with complex syntax, but various linguistic factors may be responsible for this finding, including syntactic movement, working-memory demands, and post hoc reanalysis. To distinguish between these, we tested the interaction of syntactic complexity and semantic reversibility in a functional magnetic resonance imaging study of sentence-picture matching. During auditory comprehension, semantic reversibility induced selective activation throughout the left perisylvian language network. In contrast, syntactic complexity (object-embedded vs. subject-embedded relative clauses) within reversible sentences engaged only the left inferior frontal gyrus (LIFG) and left precentral gyrus. Within irreversible sentences, only the LIFG was sensitive to syntactic complexity, confirming a unique role for this region in syntactic processing. Nonetheless, larger effects of reversibility itself occurred in the same regions, suggesting that full syntactic parsing may be a nonautomatic process applied as needed. Complex reversible sentences also induced enhanced signals in LIFG and left precentral regions on subsequent picture selection, but with additional recruitment of the right hemisphere homolog area (right inferior frontal gyrus) as well, suggesting that post hoc reanalysis of sentence structure, compared with initial comprehension, engages an overlapping but larger network of brain regions. These dissociable effects may offer a basis for studying the reorganization of receptive language function after brain damage.

Positron emission tomography correlates of visually-scored electroencephalographic waveforms during non-Rapid Eye Movement sleep.

Visually-scored, non-Rapid Eye Movement (REM) sleep electroencephalographic (EEG) waveform activity for each 30-s sleep scored epoch-including the number of sleep spindles, the number of K-complexes, and the percentage of delta waves occupying the epoch-was correlated with H(2)(15)O positron emission tomography. Sleep spindle correlations included positive correlations in the thalamus and right hippocampus. K-complex correlations included positive correlations in the frontomedian prefrontal cortex and cerebellum. Delta wave correlations included negative correlations in the thalamus, frontomedian prefrontal cortex, dorsal pons, and primary visual cortex. Each pattern of correlations may suggest a functional significance for these waveforms that relates to a waking outcome.

Neural mechanisms of auditory discrimination of long-duration tonal patterns: a neural modeling and fMRI study.

Language perception comprises mechanisms of perception and discrimination of auditory stimuli. An important component of auditory perception and discrimination concerns auditory objects. Many interesting auditory objects in our environment are of relatively long duration; however, the temporal window of integration of auditory cortex neurons processing these objects is very limited. Thus, it is necessary to make active use of short-term memory in order to construct and temporarily store long-duration objects. We sought to understand the mechanisms by which the brain manipulates long-duration tonal patterns, temporarily stores the segments of those patterns, and integrates them into an auditory object. We extended a previously constructed model of auditory recognition of short-duration tonal patterns by expanding the prefrontal cortically-based short-term memory module of the previous model into a memory buffer with multiple short-term memory submodules and by adding a gating module. The gating module distributes the segments of the input pattern to separate locations of the extended prefrontal cortex in an orderly fashion, allowing a subsequent comparison of the stored segments against the segments of a second pattern. In addition to simulating behavioral data and electrical activity of neurons, our model also produces simulations of the blood oxygen level dependent (BOLD) signal as obtained in fMRI studies. The results of these simulations provided us with predictions that we tested in an fMRI experiment with normal volunteers. This fMRI experiment used the same task and similar stimuli to that of the model. We compared simulated data with experimental values. We found that two brain areas, the right precentral gyrus and the left medial frontal gyrus, correlated well with our simulations of the memory gating module. Other fMRI studies of auditory perception and discrimination have also found correlation of fMRI activation of those areas with similar tasks and thus provide further support to our findings.

Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque.

The origin of brain mechanisms that support human language-whether these originated de novo in humans or evolved from a neural substrate that existed in a common ancestor-remains a controversial issue. Although the answer is not provided by the fossil record, it is possible to make inferences by studying living species of nonhuman primates. Here we identified neural systems associated with perceiving species-specific vocalizations in rhesus macaques using H(2)(15)O positron emission tomography (PET). These vocalizations evoke distinct patterns of brain activity in homologs of the human perisylvian language areas. Rather than resulting from differences in elementary acoustic properties, this activity seems to reflect higher order auditory processing. Although parallel evolution within independent primate species is feasible, this finding suggests the possibility that the last common ancestor of macaques and humans, which lived 25-30 million years ago, possessed key neural mechanisms that were plausible candidates for exaptation during the evolution of language.

Left hemispheric lateralization of brain activity during passive rhythm perception in musicians.

The nature of hemispheric specialization of brain activity during rhythm processing remains poorly understood. The locus for rhythmic processing has been difficult to identify and there have been several contradictory findings. We therefore used functional magnetic resonance imaging to study passive rhythm perception to investigate the hypotheses that rhythm processing results in left hemispheric lateralization of brain activity and is affected by musical training. Twelve musicians and 12 nonmusicians listened to regular and random rhythmic patterns. Conjunction analysis revealed a shared network of neural structures (bilateral superior temporal areas, left inferior parietal lobule, and right frontal operculum) responsible for rhythm perception independent of musical background. In contrast, random-effects analysis showed greater left lateralization of brain activity in musicians compared to nonmusicians during regular rhythm perception, particularly within the perisylvian cortices (left frontal operculum, superior temporal gyrus, inferior parietal lobule). These results suggest that musical training leads to the employment of left-sided perisylvian brain areas, typically active during language comprehension, during passive rhythm perception.

Neural bases of categorization of simple speech and nonspeech sounds.

Categorization is fundamental to our perception and understanding of the environment. However, little is known about the neural bases underlying the categorization of sounds. Using human functional magnetic resonance imaging (fMRI) we compared the brain responses to a category discrimination task with an auditory discrimination task using identical sets of sounds. Our stimuli differed along two dimensions: a speech-nonspeech dimension and a fast-slow temporal dynamics dimension. All stimuli activated regions in the primary and nonprimary auditory cortices in the temporal cortex and in the parietal and frontal cortices for the two tasks. When comparing the activation patterns for the category discrimination task to those for the auditory discrimination task, the results show that a core group of regions beyond the auditory cortices, including inferior and middle frontal gyri, dorsomedial frontal gyrus, and intraparietal sulcus, were preferentially activated for familiar speech categories and for novel nonspeech categories. These regions have been shown to play a role in working memory tasks by a number of studies. Additionally, the categorization of nonspeech sounds activated left middle frontal gyrus and right parietal cortex to a greater extent than did the categorization of speech sounds. Processing the temporal aspects of the stimuli had a greater impact on the left lateralization of the categorization network than did other factors, particularly in the inferior frontal gyrus, suggesting that there is no inherent left hemisphere advantage in the categorical processing of speech stimuli, or for the categorization task itself.

Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex.

Recent neuroimaging and neuropsychological data suggest that speech perception is supported in bilaterally auditory areas. We evaluate this issue building on well-known behavioral effects. While undergoing positron emission tomography (PET), subjects performed standard auditory tasks: direction discrimination of frequency-modulated (FM) tones, categorical perception (CP) of consonant-vowel (CV) syllables, and word/non-word judgments (lexical decision, LD). Compared to rest, the three conditions led to bilateral activation of the auditory cortices. However, lateralization patterns differed as a function of stimulus type: the LD task generated stronger responses in the left, the FM task a stronger response in the right hemisphere. Contrasts between either words or syllables versus FM were associated with significantly greater activity bilaterally in superior temporal gyrus (STG) ventro-lateral to Heschl's gyrus. These activations extended into the superior temporal sulcus (STS) and the middle temporal gyrus (MTG) and were greater in the left. The same areas were more active in the LD than the CP task. In contrast, the FM task was associated with significantly greater activity in the right lateral-posterior STG and lateral MTG. The findings argue for a view in which speech perception is mediated bilaterally in the auditory cortices and that the well-documented lateralization is likely associated with processes subsequent to the auditory analysis of speech.