Juha Salmi

Cognitive and motor loops of the human cerebro-cerebellar system

We applied fMRI and diffusion-weighted MRI to study the segregation of cognitive and motor functions in the human cerebro-cerebellar system. Our fMRI results show that a load increase in a nonverbal auditory working memory task is associated with enhanced brain activity in the parietal, dorsal premotor, and lateral prefrontal cortices and in lobules VII–VIII of the posterior cerebellum, whereas a sensory-motor control task activated the motor/somatosensory, medial prefrontal, and posterior cingulate cortices and lobules V/VI of the anterior cerebellum. The load-dependent activity in the crus I/II had a specific relationship with cognitive performance: This activity correlated negatively with load-dependent increase in RTs. This correlation between brain activity and RTs was not observed in the sensory-motor task in the activated cerebellar regions. Furthermore, probabilistic tractography analysis of the diffusion-weighted MRI data suggests that the tracts between the cerebral and the cerebellar areas exhibiting cognitive load-dependent and sensory-motor activity are mainly projected via separated pontine (feed-forward tracts) and thalamic (feedback tracts) nuclei. The tractography results also indicate that the crus I/II in the posterior cerebellum is linked with the lateral prefrontal areas activated by cognitive load increase, whereas the anterior cerebellar lobe is not. The current results support the view that cognitive and motor functions are segregated in the cerebellum. On the basis of these results and theories of the function of the cerebellum, we suggest that the posterior cerebellar activity during a demanding cognitive task is involved with optimization of the response speed.

Working memory, psychiatric symptoms, and academic performance at school

Previous studies of the relationship among working memory function, academic performance, and behavior in children have focused mainly on clinical populations. In the present study, the associations of the performance in audio- and visuospatial working memory tasks to teacher reported academic achievement and psychiatric symptoms were evaluated in a sample of fifty-five 6-13-year-old school children. Working memory function was measured by visual and auditory n-back tasks. Information on incorrect responses, reaction times, and multiple and missed responses were collected during the tasks. The childrens academic performance and behavioral and emotional status were evaluated by the Teacher Report Form. The results showed that good spatial working memory performance was associated with academic success at school. Children with low working memory performance, especially audiospatial memory, were reported to have more academic and attentional/behavioral difficulties at school than children with good working memory performance. An increased number of multiple and missed responses in the auditory and visual tasks was associated with teacher reported attentional/behavioral problems and in visual tasks with teacher reported anxiety/depressive symptoms. The results suggest that working memory deficits may underlie some learning difficulties and behavioral problems related to impulsivity, difficulties in concentration, and hyperactivity. On the other hand, it is possible that anxiety/depressive symptoms affect working memory function, as well as the ability to concentrate, leading to a lower level of academic performance at school.

Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception

Despite the abundant data on brain networks processing static social signals, such as pictures of faces, the neural systems supporting social perception in naturalistic conditions are still poorly understood. Here we delineated brain networks subserving social perception under naturalistic conditions in 19 healthy humans who watched, during 3-T functional magnetic resonance imaging (fMRI), a set of 137 short (approximately 16 s each, total 27 min) audiovisual movie clips depicting pre-selected social signals. Two independent raters estimated how well each clip represented eight social features (faces, human bodies, biological motion, goal-oriented actions, emotion, social interaction, pain, and speech) and six filler features (places, objects, rigid motion, people not in social interaction, non-goal-oriented action, and non-human sounds) lacking social content. These ratings were used as predictors in the fMRI analysis. The posterior superior temporal sulcus (STS) responded to all social features but not to any non-social features, and the anterior STS responded to all social features except bodies and biological motion. We also found four partially segregated, extended networks for processing of specific social signals: (1) a fronto-temporal network responding to multiple social categories, (2) a fronto-parietal network preferentially activated to bodies, motion, and pain, (3) a temporo-amygdalar network responding to faces, social interaction, and speech, and (4) a fronto-insular network responding to pain, emotions, social interactions, and speech. Our results highlight the role of the pSTS in processing multiple aspects of social information, as well as the feasibility and efficiency of fMRI mapping under conditions that resemble the complexity of real life.

Brain networks of bottom-up triggered and top-down controlled shifting of auditory attention

During functional magnetic resonance imaging (fMRI), our participants selectively attended to tone streams at the left or right, and occasionally shifted their attention from one stream to another as guided by a centrally presented visual cue. Duration changes in the to-be-attended stream served as targets. Loudness deviating tones (LDTs) occurred infrequently in both streams to catch attention in a bottom-up manner, as indicated by their effects on reaction times to targets. LDTs activated the right temporo-parietal junction (TPJ), posterior parts of the left inferior/middle frontal gyrus (IFG/MFG), ventromedial parts of the superior parietal lobule (SPL), and left frontal eye field/premotor cortex (FEF/PMC). In addition, LDTs in the to-be-ignored sound stream were associated with enhanced activity in the ventromedial prefrontal cortex (VMPFC) possibly related to evaluation of the distracting event. Top-down controlled cue-guided attention shifts (CASs) activated bilateral areas in the SPL, intraparietal sulcus (IPS), FEF/PMC, TPJ, IFG/MFG, and cingulate/medial frontal gyrus, and crus I/II of the cerebellum. Thus, our results suggest that in audition top-down controlled and bottom-up triggered shifting of attention activate largely overlapping temporo-parietal, superior parietal and frontal areas. As the IPS, superior parts of the SPL, and crus I/II were activated specifically by top-down controlled attention shifts, and the VMPFC was specifically activated by bottom-up triggered attention shifts, our results also suggest some differences between auditory top-down controlled and bottom-up triggered shifting of attention.

Functional magnetic resonance imaging phase synchronization as a measure of dynamic functional connectivity

Functional brain activity and connectivity have been studied by calculating intersubject and seed-based correlations of hemodynamic data acquired with functional magnetic resonance imaging (fMRI). To inspect temporal dynamics, these correlation measures have been calculated over sliding time windows with necessary restrictions on the length of the temporal window that compromises the temporal resolution. Here, we show that it is possible to increase temporal resolution by using instantaneous phase synchronization (PS) as a measure of dynamic (time-varying) functional connectivity. We applied PS on an fMRI dataset obtained while 12 healthy volunteers watched a feature film. Narrow frequency band (0.04-0.07 Hz) was used in the PS analysis to avoid artifactual results. We defined three metrics for computing time-varying functional connectivity and time-varying intersubject reliability based on estimation of instantaneous PS across the subjects: (1) seed-based PS, (2) intersubject PS, and (3) intersubject seed-based PS. Our findings show that these PS-based metrics yield results consistent with both seed-based correlation and intersubject correlation methods when inspected over the whole time series, but provide an important advantage of maximal single-TR temporal resolution. These metrics can be applied both in studies with complex naturalistic stimuli (e.g., watching a movie or listening to music in the MRI scanner) and more controlled (e.g., event-related or blocked design) paradigms. A MATLAB toolbox FUNPSY ( http://becs.aalto.fi/bml/software.html ) is openly available for using these metrics in fMRI data analysis.

Orienting and maintenance of spatial attention in audition and vision: multimodal and modality-specific brain activations

We studied orienting and maintenance of spatial attention in audition and vision. Functional magnetic resonance imaging (fMRI) in nine healthy subjects revealed activations in the same superior and inferior parietal, and posterior prefrontal areas in the auditory and visual orienting tasks when these tasks were compared with the corresponding maintenance tasks. Attention-related activations in the thalamus and cerebellum were observed during the auditory orienting and maintenance tasks and during the visual orienting task. In addition to the supratemporal auditory cortices, auditory orienting, and maintenance produced stronger activity than the respective visual tasks in the inferior parietal and prefrontal cortices, whereas only the occipital visual cortex and the superior parietal cortex showed stronger activity during the visual tasks than during the auditory tasks. Differences between the brain networks involved in auditory and visual spatial attention could be, for example, due to different encoding of auditory and visual spatial information or differences in stimulus-driven (bottom-up triggered) and voluntary (top-down controlled) attention between the auditory and visual modalities, or both.

Stimulus-related independent component and voxel-wise analysis of human brain activity during free viewing of a feature film.

Understanding how the brain processes stimuli in a rich natural environment is a fundamental goal of neuroscience. Here, we showed a feature film to 10 healthy volunteers during functional magnetic resonance imaging (fMRI) of hemodynamic brain activity. We then annotated auditory and visual features of the motion picture to inform analysis of the hemodynamic data. The annotations were fitted to both voxel-wise data and brain network time courses extracted by independent component analysis (ICA). Auditory annotations correlated with two independent components (IC) disclosing two functional networks, one responding to variety of auditory stimulation and another responding preferentially to speech but parts of the network also responding to non-verbal communication. Visual feature annotations correlated with four ICs delineating visual areas according to their sensitivity to different visual stimulus features. In comparison, a separate voxel-wise general linear model based analysis disclosed brain areas preferentially responding to sound energy, speech, music, visual contrast edges, body motion and hand motion which largely overlapped the results revealed by ICA. Differences between the results of IC- and voxel-based analyses demonstrate that thorough analysis of voxel time courses is important for understanding the activity of specific sub-areas of the functional networks, while ICA is a valuable tool for revealing novel information about functional connectivity which need not be explained by the predefined model. Our results encourage the use of naturalistic stimuli and tasks in cognitive neuroimaging to study how the brain processes stimuli in rich natural environments.

The brains of high functioning autistic individuals do not synchronize with those of others

Multifaceted and idiosyncratic aberrancies in social cognition characterize autism spectrum disorders (ASDs). To advance understanding of underlying neural mechanisms, we measured brain hemodynamic activity with functional magnetic resonance imaging (fMRI) in individuals with ASD and matched-pair neurotypical (NT) controls while they were viewing a feature film portraying social interactions. Pearsons correlation coefficient was used as a measure of voxelwise similarity of brain activity (InterSubject Correlations—ISCs). Individuals with ASD showed lower ISC than NT controls in brain regions implicated in processing social information including the insula, posterior and anterior cingulate cortex, caudate nucleus, precuneus, lateral occipital cortex, and supramarginal gyrus. Curiously, also within NT group, autism-quotient scores predicted ISC in overlapping areas, including, e.g., supramarginal gyrus and precuneus. In ASD participants, functional connectivity was decreased between the frontal pole and the superior frontal gyrus, angular gyrus, superior parietal lobule, precentral gyrus, precuneus, and anterior/posterior cingulate gyrus. Taken together these results suggest that ISC and functional connectivity measure distinct features of atypical brain function in high-functioning autistic individuals during free viewing of acted social interactions. Our ISC results suggest that the minds of ASD individuals do not ‘tick together’ with others while perceiving identical dynamic social interactions.

Orienting and maintenance of spatial attention in audition and vision: an event-related brain potential study

We examined the effects of orienting and maintenance of attention on performance and event‐related brain potentials (ERPs) in audition and vision. Our subjects selectively attended to sounds or pictures in one location (Maintenance of attention) or alternated the focus of their auditory or visual attention between left and right locations (Orienting of attention) in order to detect and press a response button to infrequent targets among the attended stimuli. Reaction times were longer in the Auditory Orienting condition and hit rates were lower and false alarm rates higher in the Visual Orienting condition than in the corresponding Maintenance conditions. Comparison of ERPs to the attended and unattended stimuli in the Auditory and Visual Orienting and Maintenance conditions revealed attention‐related modulations of ERPs. In each modality, ERPs to attended stimuli were negatively displaced in relation to unattended stimuli at 100–250 ms from stimulus onset. These negative differences (Nds) showed modality‐specific distributions and they were larger over the hemisphere contralateral to the attended sounds and pictures than over the ipsilateral hemisphere. Moreover, the Nd was larger in the Auditory Orienting condition than in the Auditory Maintenance condition, while no such difference was observed in the visual modality. In addition to the Nd, attended visual stimuli elicited a late positive response (LPR) in both Orienting and Maintenance conditions. In contrast to our recent functional magnetic resonance imaging (fMRI) study employing the same experimental paradigm and indicating orienting‐related activity in the frontal and parietal cortices, no ERP responses specifically related to orienting were found in either modality.

Selective attention to sound location or pitch studied with event-related brain potentials and magnetic fields

Event‐related brain potentials (ERPs) and magnetic fields (ERFs) were used to compare brain activity associated with selective attention to sound location or pitch in humans. Sixteen healthy adults participated in the ERP experiment, and 11 adults in the ERF experiment. In different conditions, the participants focused their attention on a designated sound location or pitch, or pictures presented on a screen, in order to detect target sounds or pictures among the attended stimuli. In the Attend Location condition, the location of sounds varied randomly (left or right), while their pitch (high or low) was kept constant. In the Attend Pitch condition, sounds of varying pitch (high or low) were presented at a constant location (left or right). Consistent with previous ERP results, selective attention to either sound feature produced a negative difference (Nd) between ERPs to attended and unattended sounds. In addition, ERPs showed a more posterior scalp distribution for the location‐related Nd than for the pitch‐related Nd, suggesting partially different generators for these Nds. The ERF source analyses found no source distribution differences between the pitch‐related Ndm (the magnetic counterpart of the Nd) and location‐related Ndm in the superior temporal cortex (STC), where the main sources of the Ndm effects are thought to be located. Thus, the ERP scalp distribution differences between the location‐related and pitch‐related Nd effects may have been caused by activity of areas outside the STC, perhaps in the inferior parietal regions.