Cortical Information Processing Research Articles

Unsupervised Characterization of Prediction Error Markers in Unisensory and Multisensory Streams Reveal the Spatiotemporal Hierarchy of Cortical Information Processing.

Elicited upon violation of regularity in stimulus presentation, mismatch negativity (MMN) reflects the brain's ability to perform automatic comparisons between consecutive stimuli and provides an electrophysiological index of sensory error detection whereas P300 is associated with cognitive processes such as updating of the working memory. To date, there has been extensive research on the roles of MMN and P300 individually, because of their potential to be used as clinical markers of consciousness and attention, respectively. Here, we intend to explore with an unsupervised and rigorous source estimation approach, the underlying cortical generators of MMN and P300, in the context of prediction error propagation along the hierarchies of brain information processing in healthy human participants. The existing methods of characterizing the two ERPs involve only approximate estimations of their amplitudes and latencies based on specific sensors of interest. Our objective is twofold: first, we introduce a novel data-driven unsupervised approach to compute latencies and amplitude of ERP components accurately on an individual-subject basis and reconfirm earlier findings. Second, we demonstrate that in multisensory environments, MMN generators seem to reflect a significant overlap of "modality-specific" and "modality-independent" information processing while P300 generators mark a shift toward completely "modality-independent" processing. Advancing earlier understanding that multisensory contexts speed up early sensory processing, our study reveals that temporal facilitation extends to even the later components of prediction error processing, using EEG experiments. Such knowledge can be of value to clinical research for characterizing the key developmental stages of lifespan aging, schizophrenia, and depression.

Markov Blankets and Mirror Symmetries-Free Energy Minimization and Mesocortical Anatomy.

A theoretical account of development in mesocortical anatomy is derived from the free energy principle, operating in a neural field with both Hebbian and anti-Hebbian neural plasticity. An elementary structural unit is proposed, in which synaptic connections at mesoscale are arranged in paired patterns with mirror symmetry. Exchanges of synaptic flux in each pattern form coupled spatial eigenmodes, and the line of mirror reflection between the paired patterns operates as a Markov blanket, so that prediction errors in exchanges between the pairs are minimized. The theoretical analysis is then compared to the outcomes from a biological model of neocortical development, in which neuron precursors are selected by apoptosis for cell body and synaptic connections maximizing synchrony and also minimizing axonal length. It is shown that this model results in patterns of connection with the anticipated mirror symmetries, at micro-, meso- and inter-arial scales, among lateral connections, and in cortical depth. This explains the spatial organization and functional significance of neuron response preferences, and is compatible with the structural form of both columnar and noncolumnar cortex. Multi-way interactions of mirrored representations can provide a preliminary anatomically realistic model of cortical information processing.

Evolution of neuronal cell classes and types in the vertebrate retina

The basic plan of the retina is conserved across vertebrates, yet species differ profoundly in their visual needs1. Retinal cell types may have evolved to accommodate these varied needs, but this has not been systematically studied. Here we generated and integrated single-cell transcriptomic atlases of the retina from 17 species: humans, two non-human primates, four rodents, three ungulates, opossum, ferret, tree shrew, a bird, a reptile, a teleost fish and a lamprey. We found high molecular conservation of the six retinal cell classes (photoreceptors, horizontal cells, bipolar cells, amacrine cells, retinal ganglion cells (RGCs) and Müller glia), with transcriptomic variation across species related to evolutionary distance. Major subclasses were also conserved, whereas variation among cell types within classes or subclasses was more pronounced. However, an integrative analysis revealed that numerous cell types are shared across species, based on conserved gene expression programmes that are likely to trace back to an early ancestral vertebrate. The degree of variation among cell types increased from the outer retina (photoreceptors) to the inner retina (RGCs), suggesting that evolution acts preferentially to shape the retinal output. Finally, we identified rodent orthologues of midget RGCs, which comprise more than 80% of RGCs in the human retina, subserve high-acuity vision, and were previously believed to be restricted to primates2. By contrast, the mouse orthologues have large receptive fields and comprise around 2% of mouse RGCs. Projections of both primate and mouse orthologous types are overrepresented in the thalamus, which supplies the primary visual cortex. We suggest that midget RGCs are not primate innovations, but are descendants of evolutionarily ancient types that decreased in size and increased in number as primates evolved, thereby facilitating high visual acuity and increased cortical processing of visual information.

Relationship between speech perception and cortical temporal information processing in noise

It has been known for many years that some listeners with normal hearing report difficulties in speech reception under the presence of competing sounds. The symptom is called hidden hearing loss. For the elucidation of the mechanism of hidden hearing loss, we examined the relationship between speech-in-noise reception performance and cortical temporal information processing. It has been reported that delta and theta oscillations were phase-locked to speech envelopes, and the synchronization depends on the intelligibility of degraded synthesized speech. However, it remains unclear whether and how the slow oscillations reflect speech-in-noise reception performances. We measured slow-rate (below 8 Hz) electroencephalogram (EEG) oscillations during speech reception under noise with different signal-to-noise ratio (-5 dB to -14 dB). In a control condition, EEG oscillations were measured by the same stimuli, but the participants watched a self-selected movie with subtitles, ignoring the stimuli. The power of the EEG oscillations during speech reception was stronger than those while participants ignored the stimuli. However, we did not find any dependences of the slow EEG oscillations on speech intelligibility changes associated with varying SNR. The enhancement of slow oscillations can be triggered by attention but is not likely to reflect listening effort driven by noise contamination.

Changes in Taste Perception in Patients with Minor and Major Cognitive Impairment Linked to Alzheimer's Disease Recorded by Gustatory Evoked Potentials.

The need for early diagnosis biomarkers in Alzheimer's disease (AD) is growing. Only few studies have reported gustatory dysfunctions in AD using subjective taste tests. The main purpose of the study was to explore gustatory functions using subjective taste tests and recordings of gustatory evoked potentials (GEPs) for sucrose solution in patients with minor or major cognitive impairment (CI) linked to AD, and to compare them with healthy controls. The secondary objective was to evaluate the relationships between GEPs and the results of cognitive assessments and fasting blood samples. A total of 45 subjects (15 healthy subjects, 15 minor CI patients, 15 major CI patients) were included to compare their gustatory functions and brain activity by recording GEPs in response to a sucrose stimulation. CI groups were combined in second analyses in order to keep a high power in the study. Correlations were made with cognitive scores and hormone levels (ghrelin, leptin, insulin, serotonin). Increased P1 latencies and reduced N1 amplitudes were observed in minor or major patients compared to controls. GEPs were undetectable in 6 major and 4 minor CI patients. Thresholds for sucrose detection were significantly higher in the major CI group than in controls or the minor CI group. No correlation was found with hormone levels. The cortical processing of sensory taste information seems to be altered in patients with minor or major CI linked to AD. This disturbance was identifiable with subjective taste tests only later, at the major CI stage.

The non-specific matrix thalamus facilitates the cortical information processing modes relevant for conscious awareness

The neurobiological mechanisms of arousal and anesthesia remain poorly understood. Recent evidence highlights the key role of interactions between the cerebral cortex and the diffusely projecting matrix thalamic nuclei. Here, we interrogate these processes in a whole-brain corticothalamic neural mass model endowed with targeted and diffusely projecting thalamocortical nuclei inferred from empirical data. This model captures key features seen in propofol anesthesia, including diminished network integration, lowered state diversity, impaired susceptibility to perturbation, and decreased corticocortical coherence. Collectively, these signatures reflect a suppression of information transfer across the cerebral cortex. We recover these signatures of conscious arousal by selectively stimulating the matrix thalamus, recapitulating empirical results in macaque, as well as wake-like information processing states that reflect the thalamic modulation of large-scale cortical attractor dynamics. Our results highlight the role of matrix thalamocortical projections in shaping many features of complex cortical dynamics to facilitate the unique communication states supporting conscious awareness.

Spatiotemporal characteristics of cortical activities of REM sleep behavior disorder revealed by explainable machine learning using 3D convolutional neural network

Isolated rapid eye movement sleep behavior disorder (iRBD) is a sleep disorder characterized by dream enactment behavior without any neurological disease and is frequently accompanied by cognitive dysfunction. The purpose of this study was to reveal the spatiotemporal characteristics of abnormal cortical activities underlying cognitive dysfunction in patients with iRBD based on an explainable machine learning approach. A convolutional neural network (CNN) was trained to discriminate the cortical activities of patients with iRBD and normal controls based on three-dimensional input data representing spatiotemporal cortical activities during an attention task. The input nodes critical for classification were determined to reveal the spatiotemporal characteristics of the cortical activities that were most relevant to cognitive impairment in iRBD. The trained classifiers showed high classification accuracy, while the identified critical input nodes were in line with preliminary knowledge of cortical dysfunction associated with iRBD in terms of both spatial location and temporal epoch for relevant cortical information processing for visuospatial attention tasks.

Neurophysiological measures of auditory sensory processing are associated with adaptive behavior in children with Autism Spectrum Disorder

BackgroundAtypical auditory cortical processing is consistently found in scalp electrophysiological and magnetoencephalographic studies of Autism Spectrum Disorder (ASD), and may provide a marker of neuropathological brain development. However, the relationship between atypical cortical processing of auditory information and adaptive behavior in ASD is not yet well understood.MethodsWe sought to test the hypothesis that early (100-175 ms) auditory processing in ASD is related to everyday adaptive behavior through the examination of auditory event-related potentials (AEPs) in response to simple tones and Vineland Adaptive Behavior Scales in a large cohort of children with ASD (N = 84), aged 6–17, and in age- and IQ- matched neurotypically (NT) developing controls (N = 132).ResultsStatistical analyses revealed significant group differences in early AEPs over temporal scalp regions (150-175 ms), and the expected rightward lateralization of the AEP (100-125 ms and 150-175 ms) to tonal stimuli in both groups. Lateralization of the AEP (150-175 ms) was significantly associated with adaptive functioning in the socialization domain.ConclusionsThese results lend support to the hypothesis that atypical processing of sensory information is related to everyday adaptive behavior in autism.

Normal connectivity of thalamorecipient networks in barrel equivalents of the reeler cortex.

The reeler mouse mutant has long served as a primary model to study the development of cortical layers, which is governed by the extracellular glycoprotein reelin secreted by Cajal-Retzius cells. Because layers organize local and long-range circuits for sensory processing, we investigated whether intracortical connectivity is compromised by reelin deficiency in this model. We generated a transgenic reeler mutant (we used both sexes), in which layer 4-fated spiny stellate neurons are labeled with tdTomato and applied slice electrophysiology and immunohistochemistry with synaptotagmin-2 to study the circuitry between the major thalamorecipient cell types, namely excitatory spiny stellate and inhibitory fast-spiking (putative basket) cells. In the reeler mouse, spiny stellate cells are clustered into barrel equivalents. In these clusters, we found that intrinsic physiology, connectivity, and morphology of spiny stellate and fast-spiking, putative basket cells does not significantly differ between reeler and controls. Properties of unitary connections, including connection probability, were very comparable in excitatory cell pairs and spiny stellate/fast-spiking cell pairs, suggesting an intact excitation-inhibition balance at the first stage of cortical sensory information processing. Together with previous findings, this suggests that thalamorecipient circuitry in the barrel cortex develops and functions independently of proper cortical lamination and postnatal reelin signaling.

Cortical processing during robot and functional electrical stimulation.

Like alpha rhythm, the somatosensory mu rhythm is suppressed in the presence of somatosensory inputs by implying cortical excitation. Sensorimotor rhythm (SMR) can be classified into two oscillatory frequency components: mu rhythm (8-13 Hz) and beta rhythm (14-25 Hz). The suppressed/enhanced SMR is a neural correlate of cortical activation related to efferent and afferent movement information. Therefore, it would be necessary to understand cortical information processing in diverse movement situations for clinical applications. In this work, the EEG of 10 healthy volunteers was recorded while fingers were moved passively under different kinetic and kinematic conditions for proprioceptive stimulation. For the kinetics aspect, afferent brain activity (no simultaneous volition) was compared under two conditions of finger extension: (1) generated by an orthosis and (2) generated by the orthosis simultaneously combined and assisted with functional electrical stimulation (FES) applied at the forearm muscles related to finger extension. For the kinematic aspect, the finger extension was divided into two phases: (1) dynamic extension and (2) static extension (holding the extended position). In the kinematic aspect, both mu and beta rhythms were more suppressed during a dynamic than a static condition. However, only the mu rhythm showed a significant difference between kinetic conditions (with and without FES) affected by attention to proprioception after transitioning from dynamic to static state, but the beta rhythm was not. Our results indicate that mu rhythm was influenced considerably by muscle kinetics during finger movement produced by external devices, which has relevant implications for the design of neuromodulation and neurorehabilitation interventions.

Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia.

Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and modification, and rigorous information theoretic measures for these components exist. However, the distributed computation is often also linked to neural dynamics exhibiting distinct rhythms. Thus, it would be beneficial to associate the above components of information processing with distinct rhythmic processes where possible. Here we focus on the storage of information in neural dynamics and introduce a novel spectrally-resolved measure of active information storage (AIS). Drawing on intracortical recordings of neural activity in ferrets under anesthesia before and after loss of consciousness (LOC) we show that anesthesia- related modulation of AIS is highly specific to different frequency bands and that these frequency-specific effects differ across cortical layers and brain regions. We found that in the high/low gamma band the effects of anesthesia result in AIS modulation only in the supergranular layers, while in the alpha/beta band the strongest decrease in AIS can be seen at infragranular layers. Finally, we show that the increase of spectral power at multiple frequencies, in particular at alpha and delta bands in frontal areas, that is often observed during LOC ('anteriorization') also impacts local information processing-but in a frequency specific way: Increases in isoflurane concentration induced a decrease in AIS in the alpha frequencies, while they increased AIS in the delta frequency range < 2Hz. Thus, the analysis of spectrally-resolved AIS provides valuable additional insights into changes in cortical information processing under anaesthesia.

Arousal system stimulation and anesthetic state alter visuoparietal connectivity.

Cortical information processing is under the precise control of the ascending arousal system (AAS). Anesthesia suppresses cortical arousal that can be mitigated by exogenous stimulation of the AAS. The question remains to what extent cortical information processing is regained by AAS stimulation. We investigate the effect of electrical stimulation of the nucleus Pontis Oralis (PnO), a distinct source of ascending AAS projections, on cortical functional connectivity (FC) and information storage at mild, moderate, and deep anesthesia. Local field potentials (LFPs) recorded previously in the secondary visual cortex (V2) and the adjacent parietal association cortex (PtA) in chronically instrumented unrestrained rats. We hypothesized that PnO stimulation would induce electrocortical arousal accompanied by enhanced FC and active information storage (AIS) implying improved information processing. In fact, stimulation reduced FC in slow oscillations (0.3-2.5 Hz) at low anesthetic level and increased FC at high anesthetic level. These effects were augmented following stimulation suggesting stimulus-induced plasticity. The observed opposite stimulation-anesthetic impact was less clear in the γ-band activity (30-70 Hz). In addition, FC in slow oscillations was more sensitive to stimulation and anesthetic level than FC in γ-band activity which exhibited a rather constant spatial FC structure that was symmetric between specific, topographically related sites in V2 and PtA. Invariant networks were defined as a set of strongly connected electrode channels, which were invariant to experimental conditions. In invariant networks, stimulation decreased AIS and increasing anesthetic level increased AIS. Conversely, in non-invariant (complement) networks, stimulation did not affect AIS at low anesthetic level but increased it at high anesthetic level. The results suggest that arousal stimulation alters cortical FC and information storage as a function of anesthetic level with a prolonged effect beyond the duration of stimulation. The findings help better understand how the arousal system may influence information processing in cortical networks at different levels of anesthesia.

Coordinated anatomical and functional variability in the human brain during adolescence.

Adolescence represents a time of unparalleled brain development. In particular, developmental changes in morphometric and cytoarchitectural features are accompanied by maturation in the functional connectivity (FC). Here, we examined how three facets of the brain, including myelination, cortical thickness (CT), and resting-state FC, interact in children between the ages of 10 and 15. We investigated the pattern of coordination in these measures by computing correlation matrices for each measure as well as meta-correlations among them both at the regional and network levels. The results revealed consistently higher meta-correlations among myelin, CT, and FC in the sensory-motor cortical areas than in the association cortical areas. We also found that these meta-correlations were stable and little affected by age-related changes in each measure. In addition, regional variations in the meta-correlations were consistent with the previously identified gradient in the FC and therefore reflected the hierarchy of cortical information processing, and this relationship persists in the adult brain. These results demonstrate that heterogeneity in FC among multiple cortical areas are closely coordinated with the development of cortical myelination and thickness during adolescence.

Proprioception and Geriatric Low Back Pain.

Proprioception is a deep sensation that perceives the position of each part of the body, state of movement and muscle contraction, and resistance and mass applied to the body. Proprioceptive feedback influences movement and positional accuracy, resulting in key somatosensory functions for human postural control. Proprioception encompasses signals received from proprioceptors located in the skin, subcutaneous tissue, muscles, tendons, and joint capsules, commonly known as mechanoreceptors. The muscle spindle, a crucial proprioceptor, is stretched during eccentric contraction of muscle, thus generating an action potential on afferent fibers to convey a proprioceptive information to the sensorimotor cortex in the brain. For exercise therapy in patients with locomotor disease, proprioception serves an essential function for motor control; thus, this should be considered to obtain effective muscle output. As postural control is achieved by proprioceptive function according to the balance between the lower limb and trunk, relative proprioceptive weighting ratio can help clarify proprioceptive control using muscle response to mechanical vibration. The absence of proprioceptive information congruent with motor intention activates cortical center monitoring incongruence of sensation, leading to pathological pain. Therapeutic procedures may aim to restore the integrity of cortical information processing in musculoskeletal chronic pain. Poor proprioception is one of the main causes of decreased postural balance control in elderly patients with low back pain (LBP). It has been hypothesized that proprioception of the lower limbs deteriorates with age-related muscle mass loss (sarcopenia), which increases the proprioceptive burden on the lumbar spine. Accurate diagnosis of the proprioceptive function is important for establishing a treatment procedure for proprioceptive recovery, and further prospective research is required to clarify the relationship between proprioception and LBP improvement.

Spatial organization of neuron-astrocyte interactions in the somatosensory cortex.

Microcircuits in the neocortex are functionally organized along layers and columns, which are the fundamental modules of cortical information processing. While the function of cortical microcircuits has focused on neuronal elements, much less is known about the functional organization of astrocytes and their bidirectional interaction with neurons. Here, we show that Cannabinoid type 1 receptor (CB1R)-mediated astrocyte activation by neuron-released endocannabinoids elevate astrocyte Ca2+ levels, stimulate ATP/adenosine release as gliotransmitters, and transiently depress synaptic transmission in layer 5 pyramidal neurons at relatively distant synapses (˃20μm) from the stimulated neuron. This astrocyte-mediated heteroneuronal synaptic depression occurred between pyramidal neurons within a cortical column and was absent in neurons belonging to adjacent cortical columns. Moreover, this form of heteroneuronal synaptic depression occurs between neurons located in particular layers, following a specific connectivity pattern that depends on a layer-specific neuron-to-astrocyte signaling. These results unravel the existence of astrocyte-mediated nonsynaptic communication between cortical neurons and that this communication is column- and layer-specific, which adds further complexity to the intercellular signaling processes in the neocortex.

Can you hear me now? Momentary increase in smartphone usage enhances neural processing of task-irrelevant sound tones

According to popular belief when engaged on the smartphone surrounding information is ignored. However, emerging ideas based on laboratory-designed tasks suggest that the processing of task-irrelevant (distractor) information is enhanced when cognitive load is high as anticipated during intense periods of smartphone usage. Here we address the neural processing of task-irrelevant auditory tones while interacting with the smartphone touchscreen. We analyzed neural activity (EEG) while people (N = 24) were seated in public spaces and used their smartphones for ∼1.5 h. During this period, the number of touchscreen interactions spontaneously varied from one moment to another. The central and frontal theta-band (4–8 Hz) oscillations, an index of cognitive load, increased proportionally to the number of interactions. Moreover, an index of excitation:inhibition balance derived from the aperiodic signal components increased with the interactions. The auditory tones resulted in prominent evoked potentials with peaks at ∼50 ms, ∼100 ms, and ∼200 ms, reflecting the different cortical information processing stages. Of these, the ∼100 ms component was specifically related to the number of interactions such that the higher the number of interactions, the larger the neural signal amplitudes. Contrary to the popular notions but in keeping with emerging ideas on cognitive load, auditory information processing is enhanced with increased smartphone usage. In daily life, neural processing of the surroundings is partly shaped by the immediate cognitive demands imposed by the smartphone.

Diversity in spatial frequency, temporal frequency, and speed tuning across mouse visual cortical areas and layers.

The mouse visual system consists of several visual cortical areas thought to be specialized for different visual features and/or tasks. Previous studies have revealed differences between primary visual cortex (V1) and other higher visual areas, namely, anterolateral (AL) and posteromedial (PM), and their tuning preferences for spatial and temporal frequency. However, these differences have primarily been characterized using methods that are biased toward superficial layers of cortex, such as two-photon calcium imaging. Fewer studies have investigated cell types in deeper layers of these areas and their tuning preferences. Because superficial versus deep-layer neurons and different types of deep-layer neurons are known to have different feedforward and feedback inputs and outputs, comparing the tuning preferences of these groups is important for understanding cortical visual information processing. In this study, we used extracellular electrophysiology and two-photon calcium imaging targeted toward two different layer 5 cell classes to characterize their tuning properties in V1, AL, and PM. We find that deep-layer neurons, similar to superficial layer neurons, are also specialized for different spatial and temporal frequencies, with the strongest differences between AL and V1, and AL and PM, but not V1 and PM. However, we note that the deep-layer neuron populations preferred a larger range of SFs and TFs compared to previous studies. We also find that extratelencephalically projecting layer 5 neurons are more direction selective than intratelencephalically projecting layer 5 neurons.

TU-109. Transcranial alternating current stimulation modulates cortical processing of somatosensory information in a frequency- and time-specific manner

TU-109. Transcranial alternating current stimulation modulates cortical processing of somatosensory information in a frequency- and time-specific manner

Surface Instability Modulates Cortical Information Processing In Multi-Joint Compound Movements

Surface Instability Modulates Cortical Information Processing In Multi-Joint Compound Movements

Lateralization of early orthographic processing during natural reading is impaired in developmental dyslexia

Skilled reading requires specialized visual cortical processing of orthographic information and its impairment has been proposed as a potential correlate of compromised reading in dyslexia. However, which stage of orthographic information processing during natural reading is disturbed in dyslexics remains unexplored. Here we addressed this question by simultaneously measuring the eye movements and EEG of dyslexic and control young adults during natural reading. Isolated meaningful sentences were presented at five inter-letter spacing levels spanning the range from minimal to extra-large spacing, and participants were instructed to read the text silently at their own pace. Control participants read faster, performed larger saccades and shorter fixations compared to dyslexics. While reading speed peaked around the default letter spacing, saccade amplitude increased and fixation duration decreased with the increase of letter spacing in both groups. Lateralization of occipito-temporal fixation-related EEG activity (FREA) was found in three consecutive time intervals corresponding to early orthographic processing in control readers. Importantly, the lateralization in the time range of the first negative left occipito-temporal FREA peak was specific for first fixations and exhibited an interaction effect between reading ability and letter spacing. The interaction originated in the significant decrease of FREA lateralization at extra-large compared to default letter spacing in control readers and the lack of lateralization in both letter spacing conditions in the case of dyslexics. These findings suggest that expertise-driven hemispheric functional specialization for early orthographic processing thought to be responsible for letter identity extraction during natural reading is compromised in dyslexia.