Two cortical mechanisms support the integration of visual and auditory speech: A hypothesis and preliminary data

Visual speech (lip-reading) influences the perception of heard speech. The literature suggests at least two possible mechanisms for this influence: “direct” sensory–sensory interaction, whereby sensory signals from auditory and visual modalities are integrated directly, likely in the superior temporal sulcus, and “indirect” sensory–motor interaction, whereby visual speech is first mapped onto motor-speech representations in the frontal lobe, which in turn influences sensory perception via sensory–motor integration networks. We hypothesize that both mechanisms exist, and further that previous demonstrations of lip-reading functional activations in Broca's region and the posterior planum temporale reflect the sensory–motor mechanism. We tested one prediction of this hypothesis using fMRI. We assessed whether viewing visual speech (contrasted with facial gestures) activates the same network as a speech sensory–motor integration task (listen to and then silently rehearse speech). Both tasks activated locations within Broca's area, dorsal premotor cortex, and the posterior planum temporal (Spt), and focal regions of the STS, all of which have previously been implicated in sensory–motor integration for speech. This finding is consistent with the view that visual speech influences heard speech via sensory–motor networks. Lip-reading also activated a much wider network in the superior temporal lobe than the sensory–motor task, possibly reflecting a more direct cross-sensory integration network.     

Functional neuroanatomy of the primate isocortical motor system

The concept of the primate motor cortex based on the cytoarchitectonic subdivision into areas 4 and 6 according to Brodmann or the functional subdivision into primary motor, supplementary motor, and lateral premotor cortex has changed in recent years. Instead, this cortical region is now regarded as a complex mosaic of different areas. This review article gives an overview of the structure and function of the isocortical part of the motor cortex in the macaque and human brain. In the macaque monkey, the primary motor cortex (Brodmann’s area 4 or area F1) with its giant pyramidal or Betz cells lies immediately anterior to the central sulcus. The non-primary motor cortex (Brodmann’s area 6) lies further rostrally and can be subdivided into three groups of areas: the supplementary motor areas ”SMA proper” (area F3) and ”pre-SMA” (area F6) on the mesial cortical surface, the dorsolateral premotor cortex (areas F2 and F7) on the dorsolateral convexity, and the ventrolateral premotor cortex (areas F4 and F5) on the ventrolateral convexity. The primary motor cortex is mainly involved in controlling kinematic and dynamic parameters of voluntary movements, whereas non-primary motor areas are more related to preparing voluntary movements in response to a variety of internal or external cues. Since a structural map of the human isocortical motor system as detailed as in the macaque is not yet available, homologies between the two species have not been firmly established. There is increasing evidence, however, that a similar organizational principle (i.e., primary motor cortex, supplementary motor areas, dorso- and ventrolateral premotor cortex) also exists in humans. Imaging studies have revealed that functional gradients can be discerned within the human non-primary motor cortex. More rostral cortical regions are active when a motor task is nonroutine, whereas more routine motor actions engage more caudal areas. Accepted: 3 July 2000     

Integration of cortical areas during performance of a catching ball task

The study aimed to elucidate electrophysiological and cortical mechanisms involved in anticipatory actions when healthy subjects had to catch balls in free drop; specifically through quantitative electroencephalography (qEEG) alpha absolute power changes. Our hypothesis is that during the preparation of motor action (i.e., 2 s before ball’s drop) occurred integration among left medial frontal, left primary somatomotor and left posterior parietal cortices, showing a differentiated activity involving expectation, planning and preparedness. This hypothesis supports a lateralization of motor function. Although we contend that in right-handers the left hemisphere takes on a dominant role for the regulation of motor behavior. The sample was composed of 23 healthy subjects (13 male and 10 female), right handed, with ages varying between 25 and 40 years old (32.5 ± 7.5), absence of mental and physical illness, right handed, and do not make use of any psychoactive or psychotropic substance at the time of the study. The experiment consisted of a task of catching balls in free drop. The three-way ANOVA analysis demonstrated an interaction between moment and position in left medial frontal cortex (F3 electrode), somatomotor cortex (C3 electrode) and posterior parietal cortex (P3 electrode; p < 0.001). Summarizing, through experimental task employed, it was possible to observe integration among frontal, central and parietal regions. This integration appears to be more predominant in expectation, planning and motor preparation. In this way, it established an absolute predominance of this mechanism under the left hemisphere.     

Gamma-band oscillations in fronto-central areas during performance of a sensorimotor integration task: A qEEG coherence study

This study aimed to elucidate electrophysiological and cortical mechanisms involved in anticipatory actions when 23 healthy right-handed subjects had to catch a free falling object by qEEG gamma-band (30–100 Hz). It is involved in cognitive processes, memory, spatial/temporal and proprioceptive factors. Our hypothesis is that an increase in gamma coherence in frontal areas will be observed during moment preceding ball drop, due to their involvement in attention, planning, selection of movements, preparation and voluntary control of action and in central areas during moment after ball drop, due to their involvement in motor preparation, perception and execution of movement. However, through a paired t-test, we found an increase in gamma coherence for F3–F4 electrode pair during moment preceding ball drop and confirmed our hypothesis for C3–C4 electrode pair. We conclude that gamma plays an important role in reflecting binding of several brain areas in a complex motor task as observed in our results. Moreover, for selection of movements, preparation and voluntary control of action, motor preparation, perception and execution of movement, the integration of somatosensory and visual information is mandatory.     

The neural basis of semantic memory: evidence from semantic dementia

Semantic dementia (SD) is a syndrome of progressive impairment in semantic memory. Fifty-eight brain regions were measured in seven post mortem SD cases, ten normal controls and two disease controls (diagnosis frontotemporal dementia and motor neuron disease, FTD–MND). Manual segmentation of the whole brain has not previously been undertaken in a series of SD cases, either post mortem or during life. Widespread volume loss relative to controls was found in SD, with anterior temporal lobe regions bearing the brunt (>60% atrophy of temporopolar and perirhinal cortices bilaterally). Comparison of regional volumes in SD and FTD–MND found greater atrophy in SD only in temporopolar and perirhinal volumes. The sole region showing atrophy relative to controls in FTD–MND but not SD was motor cortex. Posterior temporal and frontal regions were not consistently affected and no significant asymmetry of atrophy was found. In summary, whole-brain regional evaluation in SD, in comparison with normal controls and FTD–MND, found anterior temporal atrophy encompassing the perirhinal cortex with relative sparing of adjacent posterior temporal regions.     

Neural Representations of Visual Words and Objects: A Functional MRI Study on the Modularity of Reading and Object Processing

There have been several studies supporting the notion of a ventral-dorsal distinction in the primate cortex for visual object processing, whereby the ventral stream specializes in object identification, and the dorsal stream is engaged during object localization and interaction. There is also a growing body of evidence supporting a ventral stream that specializes in lexical (i.e., whole-word) reading, and a dorsal stream that is engaged during sub-lexical reading (i.e., phonetic decoding). Here, we consider the extent to which word-reading processes are located in regions either intersecting with, or unique from, regions that sub-serve object processing along these streams. Object identification was contrasted with lexical-based reading, and object interaction processing (i.e., deciding how to interact with an object) was contrasted with sub-lexical reading. Our results suggest that object identification and lexical-based reading are largely ventral and modular, showing mainly unique regions of activation (parahippocampal and occipital-temporal gyri function associated with object identification, and lingual, lateral occipital, and posterior inferior temporal gyri function associated with lexical-based reading) and very little shared activation (posterior inferior frontal gyrus). Object interaction processing and phonetic decoding are largely dorsal, and show both modular regions of activation (more lateralized to the dorsal-frontal right hemisphere for pseudohomophone naming, and more to the dorsal-frontal left hemisphere for the object interaction task) as well as significant shared regions of processing (precentral gyri, left inferior frontal cortex, left postcentral gyrus, left lateral occipital cortex, and superior posterior temporal gyri). Given that the perceptual experimental conditions show primarily modular and very little shared processing, whereas the analytical conditions show both substantial modular and shared processing, we discuss a reconsideration of “modularity of mind” which involves a continuum between strictly modular processing and varying degrees of shared processing, and which also depends on the nature of the tasks compared (i.e., perceptual versus analytical).     

Obsessive-compulsive disorder: A “sensory-motor” problem?

Obsessive–compulsive disorder (OCD) is a clinically heterogeneous condition. Although its pathophysiology is not completely understood, neurophysiologic and neuroimaging data have disclosed functional abnormalities in the networks linking frontal cortex, supplementary motor and premotor areas, striatum, globus pallidus, and thalamus (CSPT circuits). By means of transcranial magnetic stimulation (TMS) it is possible to test inhibitory and excitatory circuits within motor cortex.     

Impact of expected reward on neuronal activity in prefrontal cortex,frontal and supplementary eye fields and premotor cortex

In several regions of the macaque brain, neurons fire during delayed response tasks at a rate determined by the value of the reward expected at the end of the trial. The activity of these neurons might be related either to the internal representation of the appetitive value of the expected reward or to motivation-dependent variations in the monkey's level of motor preparation or motor output. According to the first interpretation, reward-related activity should be most prominent in areas affiliated with the limbic system. According to the second interpretation, it should be most prominent in areas affiliated with the motor system. To distinguish between these alternatives, we carried out single-neuron recording while monkeys performed a memory-guided saccade task in which a visual cue presented early in each trial indicated whether the reward would be large or small. Neuronal activity accompanying task performance was monitored in the dorsolateral prefrontal cortex (PFC), the frontal eye field (FEF), a transitional zone caudal to the frontal eye field (FEF/PM), premotor cortex (PM), the supplementary eye field (SEF), and the rostral part of the supplementary motor area (SMAr). The tendency for neuronal activity to increase after cues that predicted a large reward became progressively stronger in progressively more posterior areas both in the lateral sector of the frontal lobe (PFC < FEF < FEF/PM < PM) and in the medial sector (SEF < SMAr). The very strong reward-related activity of premotor neurons was presumably attributable to the monkey's motivation-dependent level of motor preparation or motor output. This finding points to the need to determine whether reward-related activity in other nonlimbic brain areas, including dorsolateral prefrontal cortex and the dorsal striatum, genuinely represents the value of the expected reward or, alternatively, is related to motivational modulation of motor signals.     

Dorsal premotor areas of nonhuman primate: functional flexibility in time domain

A voluntary motor act requires recognition of the informational content of an instruction. An instruction may contain spatial and temporal information. The recently proved role of the monkey frontal cortex in time computation, as well as in motor preparation and motor learning, suggested that we investigate the relationship between premotor neuron discharges and the temporal feature of the visual instructions. To this purpose, we manipulated the duration of an instructional cue in a visuomotor task while recording unit activity. We found two types of premotor neurons characterised by a discharge varying in relation to the duration of the cue: (1) motor-linked neurons, with a specific premotor activity constantly bounded to the motor act; (2) short-term encoders neurons, with a premotor activity depending on the cue duration. The cue duration was the critical factor in determining the behaviour of the short-term encoders cells: when the cue ranged from 0.5 s to 1 s, they presented a preparatory activity; when the cue was longer, up to 2 s, they lost their preparatory activity; when the cue was blinked the cells anticipated their discharge. The activity changed in few trials. These data confirm and highlight the role of frontal cortex in encoding specific cues with a temporal flexibility, which may be the expression of temporal learning and represent an extended aspect of cortical plasticity in time domain.     

Organization of somatic motor inputs from the frontal lobe to the pedunculopontine tegmental nucleus in the macaque monkey

To reveal the somatotopy of the pedunculopontine tegmental nucleus that functions as a brainstem motor center, we examined the distribution patterns of corticotegmental inputs from the somatic motor areas of the frontal lobe in the macaque monkey. Based on the somatotopical map prepared by intracortical microstimulation, injections of the anterograde tracers, biotinylated dextran amine and wheat germ agglutinin-conjugated horseradish peroxidase, were made into the following motor-related areas: the primary motor cortex, the supplementary and presupplementary motor areas, the dorsal and ventral divisions of the premotor cortex, and the frontal eye field. Data obtained from the present experiments were as follows: (i) Corticotegmental inputs from orofacial, forelimb, and hindlimb representations of the primary motor cortex tended to be arranged orderly from medial to lateral in the pedunculopontine tegmental nucleus. However, the distribution areas of these inputs considerably overlapped; (ii) The major input zones from distal representations of the forelimb and hindlimb regions of the primary motor cortex were located medial to those from their proximal representations, although there was a substantial overlap between the distribution areas of distal versus proximal limb inputs; (iii) The main terminal zones from the forelimb regions of the primary motor cortex, the supplementary and presupplementary motor areas, and the dorsal and ventral divisions of the premotor cortex appeared to overlap largely in the mediolaterally middle aspect of the pedunculopontine tegmental nucleus; and (iv) Corticotegmental input from the frontal eye field was scattered over the pedunculopontine tegmental nucleus.Thus, the present results indicate that the pedunculopontine tegmental nucleus is likely to receive partly separate but essentially convergent cortical inputs not only from multiple motor-related areas representing the same body part, but also from multiple regions representing diverse body parts. This suggests that somatotopical representations are intermingled rather than segregated in the pedunculopontine tegmental nucleus.     

Executive dysfunction and gray matter atrophy in amnestic mild cognitive impairment

Recent studies have shown that impairment in executive function (EF) is common in patients with amnestic mild cognitive impairment (aMCI). However, the neuroanatomic basis of executive impairment in patients with aMCI remains unclear. In this study, multiple regression voxel-based morphometry analyses were used to examine the relationship between regional gray matter volumes and EF performance in 50 patients with aMCI and 48 healthy age-matched controls. The core EF components (response inhibition, working memory and task switching, based on the EF model of Miyake et al) were accessed with computerized tasks. Atrophic brain areas related to decreases in the three EF components in patients with aMCI were located in the frontal and temporal cortices. Within the frontal cortex, the brain region related to response inhibition was identified in the right inferior frontal gyrus. Brain regions related to working memory were located in the left anterior cingulate gyrus, left premotor cortex, and right inferior frontal gyrus, and brain regions related to task shifting were distributed in the bilateral frontal cortex. Atrophy in the right inferior frontal gyrus was most closely associated with a decrease in all three EF components in patients with aMCI. Our data, from the perspective of brain morphology, contribute to a better understanding of the role of these brain areas in the neural network of EF.     

Induced EEG alpha oscillations are related to mental rotation ability: The evidence for neural efficiency and serial processing

People with better skills in mental rotation require less time to decide about the identity of rotated images. In the present study, alphanumeric characters rotated in the frontal plane were employed to assess the relationship between rotation ability and EEG oscillatory activity. Response latency, a single valid index of performance in this task, was significantly associated with the amplitude of induced oscillations in the alpha (8–13 Hz) and the low beta band (14–20 Hz). In accordance with the neural efficiency hypothesis, less event-related desynchronization (ERD) was related to better (i.e. faster) task performance. The association between response time and ERD was observed earlier (∼600–400 ms before the response) over the parietal cortex and later (∼400–200 ms before the response) over the frontal cortex. Linear mixed-effect regression analysis confirmed that both early parietal and late frontal alpha/beta power provided significant contribution to prediction of response latency. The result indicates that two distinct serially engaged neurocognitive processes comparably contribute to mental rotation ability. In addition, we found that mental rotation-related negativity, a slow event-related potential recorded over the posterior cortex, was unrelated to the asymmetry of alpha amplitude modulation.     

Dysfunctions within limbic–motor networks in amyotrophic lateral sclerosis

Previous studies have shown that affective symptoms are part of the clinical picture in amyotrophic lateral sclerosis (ALS), the most common motor neuron disorder in elderly people. Diffuse neurodegeneration of limbic regions (e.g., prefrontal cortex [PFC], amygdala) was demonstrated in ALS post-mortem, although the mechanisms of emotional dysregulation in ALS in vivo remain unclear. Using functional imaging, we assessed the brain responses to emotional faces in 11 cognitively unimpaired ALS patients and 12 healthy controls (HCs). We tested whether regional activities and connectivity patterns in the limbic system differed between ALS patients and HCs and whether the variability in clinical measures modulated the neuroimaging data. Relative to HCs, ALS patients displayed greater activation in a series of PFC areas and altered left amygdala–PFC connectivity. Anxiety modulated the right amygdala–PFC connectivity in HCs but not in ALS patients. Reduced right premotor cortex activity and altered left amygdala–supplementary motor area connectivity were associated with longer disease duration and greater disease severity, respectively. Our findings demonstrate dysfunctions of the limbic system in ALS patients at early stages of the disease, and extend our knowledge about the interplay between emotional brain areas and the regions traditionally implicated in motor control.     

Gamma band oscillations under influence of bromazepam during a sensorimotor integration task: An EEG coherence study

The goal of the present study was to explore the dynamics of the gamma band using the coherence of the quantitative electroencephalography (qEEG) in a sensorimotor integration task and the influence of the neuromodulator bromazepam on the band behavior. Our hypothesis is that the needs of the typewriting task will demand the coupling of different brain areas, and that the gamma band will promote the binding of information. It is also expected that the neuromodulator will modify this coupling. The sample was composed of 39 healthy subjects. We used a randomized double-blind design and divided subjects into three groups: placebo (n = 13), bromazepam 3 mg (n = 13) and bromazepam 6 mg (n = 13). The two-way ANOVA analysis demonstrated a main effect for the factors condition (i.e., C4–CZ electrode pair) and moment (i.e., C3–CZ, C3–C4 and C4–CZ pairs of electrodes). We propose that the gamma band plays an important role in the binding among several brain areas in complex motor tasks and that each hemisphere is influenced in a different manner by the neuromodulator.     

Motor cortical activity during drawing movements: population representation during spiral tracing

Monkeys traced spirals on a planar surface as unitary activity was recorded from either premotor or primary motor cortex. Using the population vector algorithm, the hand's trajectory could be accurately visualized with the cortical activity throughout the task. The time interval between this prediction and the corresponding movement varied linearly with the instantaneous radius of curvature; the prediction interval was longer when the path of the finger was more curved (smaller radius). The intervals in the premotor cortex fell into two groups, whereas those in the primary motor cortex formed a single group. This suggests that the change in prediction interval is a property of a single population in primary motor cortex, with the possibility that this outcome is due to the different properties generated by the simultaneous action of separate subpopulations in premotor cortex. Electromyographic (EMG) activity and joint kinematics were also measured in this task. These parameters varied harmonically throughout the task with many of the same characteristics as those of single cortical cells. Neither the lags between joint-angular velocities and hand velocity nor the lags between EMG and hand velocity could explain the changes in prediction interval between cortical activity and hand velocity. The simple spatial and temporal relationship between cortical activity and finger trajectory suggests that the figural aspects of this task are major components of cortical activity.     

Visually cued motor synchronization: modulation of fMRI activation patterns by baseline condition

A well-known issue in functional neuroimaging studies, regarding motor synchronization, is to design suitable control tasks able to discriminate between the brain structures involved in primary time-keeper functions and those related to other processes such as attentional effort. The aim of this work was to investigate how the predictability of stimulus onsets in the baseline condition modulates the activity in brain structures related to processes involved in time-keeper functions during the performance of a visually cued motor synchronization task (VM). The rational behind this choice derives from the notion that using different stimulus predictability can vary the subject's attention and the consequently neural activity. For this purpose, baseline levels of BOLD activity were obtained from 12 subjects during a conventional-baseline condition: maintained fixation of the visual rhythmic stimuli presented in the VM task, and a random-baseline condition: maintained fixation of visual stimuli occurring randomly. fMRI analysis demonstrated that while brain areas with a documented role in basic time processing are detected independent of the baseline condition (right cerebellum, bilateral putamen, left thalamus, left superior temporal gyrus, left sensorimotor cortex, left dorsal premotor cortex and supplementary motor area), the ventral premotor cortex, caudate nucleus, insula and inferior frontal gyrus exhibited a baseline-dependent activation. We conclude that maintained fixation of unpredictable visual stimuli can be employed in order to reduce or eliminate neural activity related to attentional components present in the synchronization task.     

Sex-specific gray matter volume differences in females with developmental dyslexia

Developmental dyslexia, characterized by unexpected reading difficulty, is associated with anomalous brain anatomy and function. Previous structural neuroimaging studies have converged in reports of less gray matter volume (GMV) in dyslexics within left hemisphere regions known to subserve language. Due to the higher prevalence of dyslexia in males, these studies are heavily weighted towards males, raising the question whether studies of dyslexia in females only and using the same techniques, would generate the same findings. In a replication study of men, we obtained the same findings of less GMV in dyslexics in left middle/inferior temporal gyri and right postcentral/supramarginal gyri as reported in the literature. However, comparisons in women with and without dyslexia did not yield left hemisphere differences, and instead, we found less GMV in right precuneus and paracentral lobule/medial frontal gyrus. In boys, we found less GMV in left inferior parietal cortex (supramarginal/angular gyri), again consistent with previous work, while in girls differences were within right central sulcus, spanning adjacent gyri, and left primary visual cortex. Our investigation into anatomical variants in dyslexia replicates existing studies in males, but at the same time shows that dyslexia in females is not characterized by involvement of left hemisphere language regions but rather early sensory and motor cortices (i.e., motor and premotor cortex, primary visual cortex). Our findings suggest that models on the brain basis of dyslexia, primarily developed through the study of males, may not be appropriate for females and suggest a need for more sex-specific investigations into dyslexia.     

Neuroimaging of response interference in twins concordant or discordant for inattention and hyperactivity symptoms

Attention deficit hyperactivity disorder (ADHD) is to a large extent influenced by genetic factors, but environmental influences are considered important as well. To distinguish between functional brain changes underlying primarily genetically and environmentally mediated ADHD, we used functional magnetic resonance imaging (fMRI) to compare response interference in monozygotic twins highly concordant or discordant for attention problems (AP). AP scores were assessed longitudinally with the Child Behavior Check List attention problem scale (CBCL-AP). Response interference was measured during two executive function paradigms; a color–word Stroop and a flanker task. The neuroimaging results indicated that, across the entire sample, children with high CBCL-AP scores, relative to children with low CBCL-AP scores, showed decreased activation to response interference in dorsolateral prefrontal, parietal and temporal brain regions. Increased activation was noted in the premotor cortex and regions associated with visual selective attention processing, possibly reflecting compensatory mechanisms to maintain task performance. Specific comparisons of high and low scoring concordant twin pairs suggest that AP of genetic origin was characterized by decreased activation of the left dorsolateral prefrontal cortex during the Stroop task and right parietal lobe during the flanker task. In contrast, comparison of twins from discordant monozygotic pairs, suggests that AP of environmental origin was characterized by decreased activation in left and right temporal lobe areas, but only during Stroop interference. The finding of distinct brain activation changes to response interference in inattention/hyperactivity of “genetic” versus “environmental” origin, indicates that genetic and environmental risk factors for attention/hyperactivity problems affect the brain in different ways.     

Electrophysiological evidence against parallel motor processing during multitasking

We combined behavioral measures with electrophysiological measures of motor activation (i.e., lateralized readiness potentials, LRPs) to disentangle the relative contribution of premotor and motor processes to multitasking interference in the prioritized processing paradigm. Specifically, we presented stimuli of two tasks (primary and background task) in each trial, but participants were instructed to perform the background task only if the primary task required no response. As expected, task performance was substantially influenced by a task probability manipulation: Background task responses were faster, psychological refractory period effects were smaller, and interference from the second task (i.e., backward compatibility effects) was larger when there was a larger probability that this task required a response. Critically, stimulus-locked and response-locked LRP analyses indicate that these behavioral effects of parallel processing were not driven by background task motor processing (e.g., motoric response activation) taking place during primary task processing. Instead, the LRP results suggest that these effects were exclusively localized during premotor stages of processing (e.g., response selection). Thus, the present results generally provide evidence for multitasking accounts allowing parallel task processing during response selection, whereas the task-specific motor responses are activated in a serial manner. One plausible account is that multiple task information sources can be processed in parallel, with sharing of limited cognitive resources depending on task relevance, but a primary and still active task goal prevents motor activation related to the goals of other tasks in order to avoid outcome conflict.