Large-scale gamma-band phase synchronization and selective attention

Explaining the emergence of a coherent conscious percept and an intentional agent from the activity of distributed neurons is key to understanding how the brain produces higher cognitive processes. Gamma-band synchronization has been proposed to be a mechanism for the functional integration of neural populations that together form a transitory, large-scale, task- and/or percept-specific network. The operation of this mechanism in the context of attention orienting entails that cortical regions representing attended locations should show more gamma-band synchronization with other cortical areas than would those representing unattended locations. This increased synchronization should be apparent in the same time frame as that of the deployment of attention to a particular location. In order to observe this effect, we made electroencephalogram recordings while subjects attended to one side or the other of the visual field (which we confirmed by event-related potential analysis) and calculated phase-locking statistics between the signals recorded at relevant electrode pairs. We observed increased gamma-band phase synchronization between visual cortex contralateral to the attended location and other, widespread, cortical areas approximately 240-380 ms after the directional cue was presented, confirming the prediction of a large-scale gamma synchronous network oriented to the cued location.     

Phase coupling in a cerebro-cerebellar network at 8-13 Hz during reading

Words forming a continuous story were presented to 9 subjects at frequencies ranging from 5 to 30 Hz, determined individually to render comprehension easy, effortful, or practically impossible. We identified a left-hemisphere neural network sensitive to reading performance directly from the time courses of activation in the brain, derived from magnetoencephalography data. Regardless of the stimulus rate, communication within the long-range neural network occurred at a frequency of 8-13 Hz. Our coherence-based detection of interconnected nodes reproduced several brain regions that have been previously reported as active in reading tasks, based on traditional contrast estimates. Intriguingly, the face motor cortex and the cerebellum, typically associated with speech production, and the orbitofrontal cortex, linked to visual recognition and working memory, additionally emerged as densely connected components of the network. The left inferior occipitotemporal cortex, involved in early letter-string or word-specific processing, and the cerebellum turned out to be the main forward driving nodes of the network. Synchronization within a subset of nodes formed by the left occipitotemporal, the left superior temporal, and orbitofrontal cortex was increased with the subjects' effort to comprehend the text. Our results link long-range neural synchronization and directionality with cognitive performance.     

Dissociating neural correlates of cognitive components in mental calculation

Mental calculation is a complex cognitive operation that is composed of a set of distinct functional processes. Using functional magnetic resonance imaging (fMRI), we mapped brain activity in healthy subjects performing arithmetical tasks and control tasks evoking a comparable load on visuo-constructive, linguistic, attentional and mnemonic functions. During calculation, as well as non-mathematical tasks, similar cortical networks consisting of bilateral prefrontal, premotor and parietal regions were activated, suggesting that most of these cortical areas do not exclusively represent modules for calculation but support more general cognitive operations that are instrumental but not specific to mental arithmetic. Significant differences between calculation and the non-mathematical tasks were found in parietal sub-regions, where non-arithmetic number or letter substitution tasks preferentially activated the superior parietal lobules whereas calculation predominantly elicited activation of the left dorsal angular gyrus and the medial parietal cortices. We interpret the latter activations to reflect sub-processes of mental calculation that are related to the processing of numerical representations during exact calculation and to arithmetical fact retrieval. Finally, we found that more complex calculation tasks involving the application of calculation rules increased activity in left inferior frontal areas that are known to subserve linguistic and working memory functions. Taken together, these findings help to embed the specific cognitive operation of calculation into a neural framework that provides the required set of instrumental components. This result may further inform the cognitive modeling of calculation and adds to the understanding of neuropsychological deficit patterns in patients.     

Interactions between cortical rhythms and spiking activity of single basal ganglia neurons in the normal and parkinsonian state

In order to evaluate the specific interactions between cortical oscillations and basal ganglia-spiking activity under normal and parkinsonian conditions, we examined the relationship between frontal cortex electroencephalographic (EEG) signals and simultaneously recorded neuronal activity in the internal and external segments of the pallidum or the subthalamic nucleus (STN) in 3 rhesus monkeys. After we made recordings in the normal state, hemiparkinsonism was induced with intracarotid injections of the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in one animal, followed by additional recordings. Spiking activity in the pallidum and STN was associated with significant shifts in the level of EEG synchronization. We also found that the spectral power of beta- and gamma-band EEG rhythms covaried positively before the basal ganglia spikes but did not covary or covaried negatively thereafter. In parkinsonism, changes in cortical synchronization and phase coherence were reduced in EEG segments aligned to STN spikes, whereas both were increased in data segments aligned to pallidal spikes. Spiking-related changes in beta/gamma-band covariance were reduced. The findings indicate that basal ganglia and cortex interact in the processing of cortical rhythms that contain oscillations across a broad range of frequencies and that this interaction is severely disrupted in parkinsonism.     

Task-Induced Brain Activity Patterns in Type 2 Diabetes: A Potential Biomarker for Cognitive Decline

Patients with type 2 diabetes demonstrate reduced functional connectivity within the resting state default mode network (DMN), which may signal heightened risk for cognitive decline. In other populations at risk for cognitive decline, additional magnetic resonance imaging abnormalities are evident during task performance, including impaired deactivation of the DMN and reduced activation of task-relevant regions. We investigated whether middle-aged type 2 diabetic patients show these brain activity patterns during encoding and recognition tasks. Compared with control participants, we observed both reduced 1) activation of the dorsolateral prefrontal cortex during encoding and 2) deactivation of the DMN during recognition in type 2 diabetic patients, despite normal cognition. During recognition, activation in several task-relevant regions, including the dorsolateral prefrontal cortex and DMN regions, was positively correlated with HbA_1c and insulin resistance, suggesting that these important markers of glucose metabolism impact the brain’s response to a cognitive challenge. Plasma glucose ≥11 mmol/L was associated with impaired deactivation of the DMN, suggesting that acute hyperglycemia contributes to brain abnormalities. Since elderly type 2 diabetic patients often demonstrate cognitive impairments, it is possible that these task-induced brain activity patterns observed in middle age may signal impending cognitive decline.     

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.     

Where Is ELSA? The Early to Late Shift in Aging

Studies of cognitive and neural aging have recently provided evidence of a shift from an early- to late-onset cognitive control strategy, linked with temporally extended activity in the prefrontal cortex (PFC). It has been uncertain, however, whether this age-related shift is unique to PFC and executive control tasks or whether the functional location might vary depending on the particular cognitive processes that are altered. The present study tested whether an early-to-late shift in aging (ELSA) might emerge in the medial temporal lobes (MTL) during a protracted context memory task comprising both anticipatory cue (retrieval preparation) and retrieval probe (retrieval completion) phases. First, we found reduced MTL activity in older adults during the early retrieval preparation phase coupled with increased MTL activity during the late retrieval completion phase. Second, we found that functional connectivity between MTL and PFC regions was higher during retrieval preparation in young adults but higher during retrieval completion in older adults, suggesting an important interactive relationship between the ELSA pattern in MTL and PFC. Taken together, these results critically suggest that aging results in temporally lagged activity even in regions not typically associated with cognitive control, such as the MTL.     

The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing

One of the challenges to functional neuroimaging is to understand how the component processes of reading comprehension emerge from the neural activity in a network of brain regions. In this study, functional magnetic resonance imaging (fMRI) was used to examine lexical and syntactic processing in reading comprehension by independently manipulating the cognitive demand on each of the two processes of interest. After establishing a consistency with earlier research showing the involvement of the left perisylvian language areas in both lexical access and syntactic processing, the study produced new findings that are surprising in two ways: (i) the lexical and syntactic factors each impact not just individual areas, but they affect the activation in a network of left-hemisphere areas, suggesting that changing the computational load imposed by a given process produces a cascade of effects in a number of collaborating areas; and (ii) the lexical and syntactic factors usually interact in determining the amount of activation in each affected area, suggesting that comprehension processes that operate on different levels of language may nevertheless draw on a shared infrastructure of cortical resources. The results suggest that many processes in sentence comprehension involve multiple brain regions, and that many brain regions contribute to more than one comprehension process. The implication is that the language network consists of brain areas which each have multiple relative specializations and which engage in extensive interarea collaborations.     

Exploring the neural dynamics underpinning individual differences in sentence comprehension

This study used functional magnetic resonance imaging to investigate individual differences in the neural underpinnings of sentence comprehension, with a focus on neural adaptability (dynamic configuration of neural networks with changing task demands). Twenty-seven undergraduates, with varying working memory capacities and vocabularies, read sentences that were either syntactically simple or complex under conditions of varying extrinsic working memory demands (sentences alone or preceded by to-be-remembered words or nonwords). All readers showed greater neural adaptability when extrinsic working memory demands were low, suggesting that adaptability is related to resource availability. Higher capacity readers showed greater neural adaptability (greater increase in activation with increasing syntactic complexity) across conditions than did lower capacity readers. Higher capacity readers also showed better maintenance of or increase in synchronization of activation between brain regions as tasks became more demanding. Larger vocabulary was associated with more efficient use of cortical resources (reduced activation in frontal regions) in all conditions but was not associated with greater neural adaptability or synchronization. The distinct characterizations of verbal working memory capacity and vocabulary suggest that dynamic facets of brain function such as adaptability and synchronization may underlie individual differences in more general information processing abilities, whereas neural efficiency may more specifically reflect individual differences in language experience.     

Individual differences in anterior cingulate/paracingulate morphology are related to executive functions in healthy males

The neuropsychological correlates of inter-individual variations in cortical folding are poorly understood. Anterior cingulate (AC) cortex is one region characterized by considerable variability, particularly with respect to the paracingulate sulcus (PCS), which is present in only 30-60% of individuals and more commonly found in the left cerebral hemisphere. To investigate whether inter-individual differences in this PCS asymmetry are related to cognitive performance, we classified 30 healthy right-handed males as displaying either a leftward, rightward or symmetric pattern of folding based on the incidence and extent of the PCS in each hemisphere, and compared their performance on tasks engaging executive cognitive processes associated with frontal lobe function. We found that the more common leftward PCS asymmetry was associated with better performance across verbal and non-verbal executive tasks, but that PCS variability had no effect on tasks less dependent on executive functions. These results suggest that the leftward pattern of folding is associated with a non-specific performance advantage on cognitively demanding executive function tasks, possibly due to differences in functional interactions between AC/paracingulate cortex and connected frontal regions. It therefore appears that normal variations in brain morphology are associated with individual differences in cognitive abilities.     

Organization of language areas in bilingual patients: a cortical stimulation study

OBJECT: In an attempt to gain a better understanding of how multiple languages are represented in the human brain, the authors studied bilingual patients who underwent surgery for brain tumors, during which the authors mapped cortical language sites by using electrostimulation. METHODS: Reading, counting, and word retrieval tasks were studied in 12 right-handed bilingual patients with no language deficit. All bilingual patients were native to France. One patient spoke four languages. The patients constituted a nonhomogeneous group in terms of language proficiency or age of acquisition. Languages were evaluated and classified into three major groups, depending on proficiency and date of acquisition. Strict conditions of language site validation were applied, separating typical anomia sites from speech arrest or other language sites (such as hesitation sites). A total of 30 speech arrest sites, 16 anomia sites, and three sites of language difficulties (not typically classified as speech arrest) were found throughout the 26 language studies performed. Strict overlapping of language areas (for all language tasks) was found in five patients, whereas the remaining seven had at least one area that was language-specific and sometimes task-specific. Specific areas for a particular language were found for word retrieval tasks (anomia) in eight sites (50%) but also in six (20%) of the reading or counting sites (speech arrest), either in frontal (three patients) or in temporoparietal (four patients) regions. Among the four early bilingual patients tested (languages acquired before the age of 7 years), three had language-specific cortical areas. Interestingly, six patients in this series who had a discrepancy between two languages did not have more cortical areas devoted to the less proficient language (with acknowledgment of the limit in cortical exposure available for testing by the craniotomy). CONCLUSIONS: In this series, the authors found that bilingual patients could have common but also different cortical areas for both languages in temporoparietal areas and in frontal areas. In some cases, the authors found that language tasks such as counting, reading, or word retrieval in different languages can be sustained by language- and task-specific cortical areas. In bilingual patients, cortical mapping should ideally be performed using different language tasks in all languages in which the patient is fluent.     

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.     

Stimulus-dependent modulations of correlated high-frequency oscillations in cat visual cortex

The hypothesis that correlated neural activity is involved in the cortical representation of visual stimuli was examined by recording multi-unit activity and local field potentials from neurons with non- overlapping receptive fields in areas 17 and 18. Using coherence functions, correlations of oscillatory patterns (35-100 Hz) of neural signals were investigated under three stimulus conditions: (i) a whole field grating or a long bar moving across both receptive fields; (ii) masking the region between both receptive fields while stimulating the remaining visual field; and (iii) two separate stimuli simultaneously moving in opposite directions. Coherences of oscillations were found to be significantly higher in the first stimulus condition than in the other two conditions. Since different visual stimuli were reflected in the coherence of neural activity, we concluded that correlated neural activity is a potential candidate for coding of sensory information.      

The effects of stimulus modality and frequency of stimulus presentation on cross-modal distraction

Selective attention produces enhanced activity (attention-related modulations [ARMs]) in cortical regions corresponding to the attended modality and suppressed activity in cortical regions corresponding to the ignored modality. However, effects of behavioral context (e.g., temporal vs. spatial tasks) and basic stimulus properties (i.e., stimulus frequency) on ARMs are not fully understood. The current study used functional magnetic resonance imaging to investigate selectively attending and responding to either a visual or auditory metronome in the presence of asynchronous cross-modal distractors of 3 different frequencies (0.5, 1, and 2 Hz). Attending to auditory information while ignoring visual distractors was generally more efficient (i.e., required coordination of a smaller network) and less effortful (i.e., decreased interference and presence of ARMs) than attending to visual information while ignoring auditory distractors. However, these effects were modulated by stimulus frequency, as attempting to ignore auditory information resulted in the obligatory recruitment of auditory cortical areas during infrequent (0.5 Hz) stimulation. Robust ARMs were observed in both visual and auditory cortical areas at higher frequencies (2 Hz), indicating that participants effectively allocated attention to more rapidly presented targets. In summary, results provide neuroanatomical correlates for the dominance of the auditory modality in behavioral contexts that are highly dependent on temporal processing.     

Binding symbols and sounds: evidence from event-related oscillatory gamma-band activity

The present study intended to examine the neural basis of audiovisual integration, hypothetically achieved by synchronized gamma-band oscillations (30-80 Hz) that have been suggested to integrate stimulus features and top-down information. To that end, we studied the impact of visual symbolic information on early auditory sensory processing of upcoming sounds. In particular, we used a symbol-to-sound-matching paradigm in which simple score-like patterns predict corresponding sound patterns. Occasionally, a single sound is incongruent with the corresponding element of the visual pattern. In response to expected sounds congruent with the corresponding visual symbol, a power increase of phase-locked (evoked) activity in the 40-Hz band was observed peaking 42-ms poststimulus onset. Thus, for the first time, we demonstrated that the comparison process between a neural model, the expectation, and the current sensory input is implemented at very early levels of auditory processing. Subsequently, expected congruent sounds elicited a broadband power increase of non-phase-locked (induced) activity peaking 152-ms poststimulus onset, which might reflect the formation of a unitary event representation including both visual and auditory aspects of the stimulation. Gamma-band responses were not present for unexpected incongruent sounds. A model explaining the anticipatory activation of cortical auditory representations and the match of experience against expectation is presented.     

Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies

Damage to parietal cortex impairs visuospatial judgments. However, it is currently unknown how this damage may affect or indeed be caused by functional changes in remote but interconnected brain regions. Here, we applied transcranial magnetic stimulation (TMS) to the parietal cortices during functional magnetic resonance imaging (fMRI) while participants were solving visuospatial tasks. This allowed us to observe both the behavioral and the neural effects of transient parietal activity disruption in the active healthy human brain. Our results show that right, but not left, parietal TMS impairs visuospatial judgment, induces neural activity changes in a specific right-hemispheric network of frontoparietal regions, and shows significant correlations between the induced behavioral impairment and neural activity changes in both the directly stimulated parietal and remote ipsilateral frontal brain regions. The revealed right-hemispheric neural network effect of parietal TMS represents the same brain areas that are functionally connected during the execution of visuospatial judgments. This corroborates the notion that visuospatial deficits following parietal damage are brought about by a perturbation of activity across a specific frontoparietal network, rather than the lesioned parietal site alone. Our experiments furthermore show how concurrent fMRI and magnetic brain stimulation during active task execution hold the potential to identify and visualize networks of brain areas that are functionally related to specific cognitive processes.     

Increased neural efficiency with repeated performance of a working memory task is information-type dependent

Unlike tasks in which practice leads to an automatic stimulus-response association, it is thought working memory (WM) tasks continue to require cognitive control processes after repeated performance. Previous studies investigating WM task repetition are in accord with this. However, it is unclear whether changes in neural activity after repetition imply alterations in general control processes common to all WM tasks or are specific to the selection, encoding and maintenance of the relevant information. In the present study, functional magnetic resonance imaging (fMRI) was used to examine changes during sample, delay and test periods during repetition of both object and spatial delayed recognition tasks. We found decreases in fMRI activation in both spatial and object-selective areas after spatial WM task repetition, independent of behavioral performance. Few areas showed changed activity after object WM task repetition. These results indicate that spatial task repetition leads to increased efficiency of maintaining task-relevant information and improved ability to filter out task-irrelevant information. The specificity of this repetition effect to the spatial task suggests a difference exists in the nature of the representation of object and spatial information and that their maintenance in WM is likely subserved by different neural systems.     

Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations

Using single and multiunit recordings in the striate cortex of alert macaque monkeys, we find that gamma-band (20-70 Hz) oscillations in neuronal firing are a prominent feature of V1 neuronal activity. The properties of this rhythmic activity are very similar to those previously observed in the cat. Gamma-band activity is strongly dependent on visual stimulation, largely absent during spontaneous activity and, under the conditions of our experiment, not time-locked to the vertical refresh of the computer monitor (80 Hz) used to present the stimuli. In our sample, 61% of multiunit activity (MUA) and 46% of single-unit activity (SUA) was significantly oscillatory, with mean frequencies of 48+/-9 and 42+/-13 Hz, respectively. Gamma-band activity was most likely to occur when cells were activated by their optimal stimuli, but still occurred, although less often and with lower amplitude, in response to nonoptimal stimuli. The frequency of gamma-band activity also reflected stimulus properties, with drifting gratings evoking higher-frequency oscillations than stationary gratings. As in the cat, the spike trains of single cells showing gamma-band oscillations often displayed a pattern of repetitive burst firing, with intraburst firing rates of 300-800 Hz. The overall similarity of rhythmic neuronal activity in the primary visual cortex of cats and monkeys suggests that the phenomenon is not species-specific. The stimulus-dependence of the rhythmic activity is consistent with a functional role in visual perception.