Higher Association Cortices Research Articles

The human corticocortical vestibular network

BackgroundLittle is known about the cortical organization of human vestibular information processing. Instead of a dedicated primary vestibular cortex, a distributed network of regions across the cortex respond to vestibular input. The aim of this study is to characterize the human corticocortical vestibular network and compare it to established results in non-human primates. MethodsWe collected high-resolution multi-shell diffusion-weighted (DWI) and state-of-the-art resting-state functional MR images of 29 right-handed normal subjects. Ten cortical vestibular regions per hemisphere were predefined from previous vestibular stimulation studies and applied as regions of interest. Four different structural corticocortical vestibular networks accounting for relevant constraints were investigated. The analyses included the investigation of common network measures and hemispheric differences for functional and structural connectivity patterns alike. In addition, the results of the structural vestibular network were compared to findings previously reported in non-human primates with respect to tracer injections (Guldin and Grusser, 1998). ResultsAll structural networks independent of the applied constraints showed a recurring subdivision into identical three submodules. The structural human network was characterized by a predominantly intrahemispheric connectivity, whereas the functional pattern highlighted a strong connectivity for all homotopic nodes. A significant laterality preference towards the right hemisphere can be observed throughout the analyses: (1) with larger nodes, (2) stronger connectivity values structurally and functionally, and (3) a higher functional relevance. Similar connectivity patterns to non-human primate data were found in sensory and higher association cortices rather than premotor and motor areas. ConclusionOur analysis delineated a remarkably stable organization of cortical vestibular connectivity. Differences found between primate species may be attributed to phylogeny as well as methodological differences. With our work we solidified evidence for lateralization within the corticocortical vestibular network. Our results might explain why cortical lesions in humans do not lead to persistent vestibular symptoms. Redundant structural routing throughout the network and a high-degree functional connectivity may buffer the network and reestablish network integrity quickly in case of injury.

A Spiking Neurocomputational Model of High-Frequency Oscillatory Brain Responses to Words and Pseudowords.

Experimental evidence indicates that neurophysiological responses to well-known meaningful sensory items and symbols (such as familiar objects, faces, or words) differ from those to matched but novel and senseless materials (unknown objects, scrambled faces, and pseudowords). Spectral responses in the high beta- and gamma-band have been observed to be generally stronger to familiar stimuli than to unfamiliar ones. These differences have been hypothesized to be caused by the activation of distributed neuronal circuits or cell assemblies, which act as long-term memory traces for learned familiar items only. Here, we simulated word learning using a biologically constrained neurocomputational model of the left-hemispheric cortical areas known to be relevant for language and conceptual processing. The 12-area spiking neural-network architecture implemented replicates physiological and connectivity features of primary, secondary, and higher-association cortices in the frontal, temporal, and occipital lobes of the human brain. We simulated elementary aspects of word learning in it, focussing specifically on semantic grounding in action and perception. As a result of spike-driven Hebbian synaptic plasticity mechanisms, distributed, stimulus-specific cell-assembly (CA) circuits spontaneously emerged in the network. After training, presentation of one of the learned “word” forms to the model correlate of primary auditory cortex induced periodic bursts of activity within the corresponding CA, leading to oscillatory phenomena in the entire network and spontaneous across-area neural synchronization. Crucially, Morlet wavelet analysis of the network's responses recorded during presentation of learned meaningful “word” and novel, senseless “pseudoword” patterns revealed stronger induced spectral power in the gamma-band for the former than the latter, closely mirroring differences found in neurophysiological data. Furthermore, coherence analysis of the simulated responses uncovered dissociated category specific patterns of synchronous oscillations in distant cortical areas, including indirectly connected primary sensorimotor areas. Bridging the gap between cellular-level mechanisms, neuronal-population behavior, and cognitive function, the present model constitutes the first spiking, neurobiologically, and anatomically realistic model able to explain high-frequency oscillatory phenomena indexing language processing on the basis of dynamics and competitive interactions of distributed cell-assembly circuits which emerge in the brain as a result of Hebbian learning and sensorimotor experience.

The potential application of transcranial magnetic stimulation in ophthalmology: a brief perspective

Transcranial magnetic stimulation (TMS), while employed in both cognitive investigations and evaluated as a potential therapeutic technique for several conditions, is not widely used in ophthalmology. As a technique, one of the advantages of TMS is that it can create a “virtual lesion”, or temporary disruption of the functioning of a brain area, to facilitate investigation of the processes that the disrupted area may be involved in. In ophthalmology, higher association cortex is associated with visual cognition and control of eye movements, processes which could further be investigated using TMS experiments. This paper aims to provide a perspective of how TMS could be more broadly applied in ophthalmology.

Laminar Module Cascade from Layer 5 to 6 Implementing Cue-to-Target Conversion for Object Memory Retrieval in the Primate Temporal Cortex

The cerebral cortex computes through the canonical microcircuit that connects six stacked layers; however, how cortical processing streams operate invivo, particularly in the higher association cortex, remains elusive. By developing a novel MRI-assisted procedure that reliably localizes recorded single neurons at resolution of six individual layers in monkey temporal cortex, we show that transformation of representations from a cued object to a to-be-recalled object occurs at the infragranular layer in a visual cued-recall task. This cue-to-target conversion started in layer 5 and was followed by layer 6. Finally, a subset of layer 6 neurons exclusively encoding the sought target became phase-locked to surrounding field potentials at theta frequency, suggesting that this coordinated cell assembly implements cortical long-distance outputs of the recalled target. Thus, this study proposes a link from local computation spanning laminar modules of the temporal cortex to the brain-wide network for memory retrieval in primates.

Intersubject information mapping: revealing canonical representations of complex natural stimuli

Abstract Real-world time-continuous stimuli such as video promise greater naturalism for studies of brain function. However, modeling the stimulus variation is challenging and introduces a bias in favor of particular descriptive dimensions. Alternatively, we can look for brain regions whose signal is correlated between subjects, essentially using one subject to model another. Intersubject correlation mapping (ICM) allows us to find brain regions driven in a canonical manner across subjects by a complex natural stimulus. However, it requires a direct voxel-to-voxel match between the spatiotemporal activity patterns and is thus only sensitive to common activations sufficiently extended to match up in Talairach space (or in an alternative, e.g. cortical-surface-based, common brain space). Here we introduce the more general approach of intersubject information mapping (IIM). For each brain region, IIM determines how much information is shared between the subjects' local spatiotemporal activity patterns. We estimate the intersubject mutual information using canonical correlation analysis applied to voxels within a spherical searchlight centered on each voxel in turn. The intersubject information estimate is invariant to linear transforms including spatial rearrangement of the voxels within the searchlight. This invariance to local encoding will be crucial in exploring fine-grained brain representations, which cannot be matched up in a common space and, more fundamentally, might be unique to each individual – like fingerprints. IIM yields a continuous brain map, which reflects intersubject information in fine-grained patterns. Performed on data from functional magnetic resonance imaging (fMRI) of subjects viewing the same television show, IIM and ICM both highlighted sensory representations, including primary visual and auditory cortices. However, IIM revealed additional regions in higher association cortices, namely temporal pole and orbitofrontal cortex. These regions appear to encode the same information across subjects in their fine-grained patterns, although their spatial-average activation was not significantly correlated between subjects.

Neuromagnetic oscillations to emotional faces and prosody

Higher association cortices as well as unisensory areas can support multisensory integration [D. Senkowski et al. (2008) Trends Neurosci., 31, 401-409]. The present study investigated whether audiovisual integration of emotional information emerges early at unisensory or later at higher association cortices. Emotional stimuli were presented in three blocks: audiovisual (AV), auditory (A) and visual (V). Eighteen participants performed a delayed emotional recognition task (happy, angry or neutral prosody and/or facial expression) while whole-brain magnetoencephalography (MEG) data were obtained. Time-frequency evoked and total power analyses were performed on the sensor data, and source localization of the frequencies of interest performed via a synthetic aperture magnetometry beamformer. To examine crossmodal integration between bimodal and unimodal conditions, two contrasts were specified: AV > A and AV > V. In the AV > A contrast, early effects were observed on both the temporal and the occipital evoked responses. However, at the source level, early alpha suppression was limited to the occipital sources without changes in temporal cortices. In the AV > V contrast, sensor and source findings revealed increased alpha suppression only in temporal cortices, with no changes in visual cortex. Thus, no crossmodal effect in unisensory areas emerged. Instead, increased frontal alpha activity in both the AV > A and AV > V contrasts supports the view that affective information from face and prosody converges at higher association cortices.

Progressive plasticity of auditory cortex during appetitive operant conditioning

In stimulus–response–outcome learning, different regions in the cortico-basal ganglia network are progressively involved according to the stage of learning. However, the involvement of sensory cortex remains ellusive even though massive cortical projections to the striatum imply its significant role in this learning. Here we show that the global tonotopic representation in the auditory cortex changed progressively depending on the stage of training in auditory operant conditioning. At the early stage, tone-responsive areas mainly in the core cortex expanded, while both the core and belt cortices shrank at the late stage as behavior became conditioned. Taken together with previous findings, this progressive global plasticity from the core to belt cortices suggests differentiated roles in these areas: the core cortex serves as a filter to better identify auditory objects for hierarchical computation within the belt cortex, while the belt stores auditory objects and affects decision making through direct projections to limbic system and higher association cortex. Thus, the progressive plasticity in the present study reflects a shift from identification to storage of a behaviorally relevant auditory object, which is potentially associated with a habitual behavior.

Visual Enhancement of the Information Representation in Auditory Cortex

Combining information across different sensory modalities can greatly facilitate our ability to detect, discriminate, or recognize sensory stimuli. Although this process of sensory integration has usually been attributed to classical association cortices, recent work has demonstrated that neuronal activity in early sensory cortices can also be influenced by cross-modal inputs. Here we demonstrate that such "early" multisensory influences enhance the information carried by neurons about multisensory stimuli. By recording in auditory cortex of alert monkeys watching naturalistic audiovisual stimuli, we quantified the effect of visual influences on the trial-to-trial response variability and on the amount of information carried by neural responses. We found that firing rates and precisely timed spike patterns of individual units became more reliable across trials and time when multisensory stimuli were presented, leading to greater encoded stimulus information. Importantly, this multisensory information enhancement was much reduced when the visual stimulus did not match the sound. These results demonstrate that multisensory influences enhance information processing already at early stages in cortex, suggesting that sensory integration is a distributed process, commencing in lower sensory areas and continuing in higher association cortices.

Spatial Organization of Multisensory Responses in Temporal Association Cortex

Neurons in sensory cortices are often topographically organized according to their response preferences. We here show that such an organization of response preferences also exists in multisensory association cortex. Using electrophysiological mappings, we probed the modality preference to auditory and visual stimuli of neurons in the superior temporal association cortex of nonhuman primates. We found that neurons preferring the same modality (auditory or visual) often co-occur in close spatial proximity or occur intermingled with bimodal neurons. Neurons preferring different modalities, in contrast, occur spatially separated. This organization at the scale of individual neurons leads to extended patches of same modality preference when analyzed at the scale of millimeters, revealing larger-scale regions that preferentially respond to the same modality. In addition, we find that neurons exhibiting signs of multisensory interactions, such as superadditive or subadditive response summation, also occur in spatial clusters. Together, these results reveal a spatial organization of modality preferences in a higher association cortex and lend support to the notion that topographical organizations might serve as a general principle of integrating information within and across the sensory modalities.

Multisensory interactions in primate auditory cortex: fMRI and electrophysiology

Recent studies suggest that multisensory integration does not only occur in higher association cortices but also at early stages of auditory processing, possibly in primary or secondary auditory cortex. Support for such early multisensory influences comes from functional magnetic resonance imaging experiments in humans and monkeys. However we argue that the current understanding of neurovascular coupling and of the neuronal basis underlying the imaging signal does not permit the direct extrapolation from imaging data to properties of neurons in the same region. While imaging can guide subsequent electrophysiological studies, only these can determine whether and how neurons in auditory cortices combine information from multiple modalities. Indeed, electrophysiological studies only partly confirm the findings from imaging studies. While recordings of field potentials reveal strong influences of visual or somatosensory stimulation on synaptic activity even in primary auditory cortex, single unit studies find only a small minority of neurons as being influenced by non-acoustic stimuli. We propose the analysis of the information coding properties of individual neurons as one way to quantitatively determine whether the representation of our acoustic environment in (primary) auditory cortex indeed benefits from multisensory input.

Functional Imaging Reveals Visual Modulation of Specific Fields in Auditory Cortex

Merging the information from different senses is essential for successful interaction with real-life situations. Indeed, sensory integration can reduce perceptual ambiguity, speed reactions, or change the qualitative sensory experience. It is widely held that integration occurs at later processing stages and mostly in higher association cortices; however, recent studies suggest that sensory convergence can occur in primary sensory cortex. A good model for early convergence proved to be the auditory cortex, which can be modulated by visual and tactile stimulation; however, given the large number and small size of auditory fields, neither human imaging nor microelectrode recordings have systematically identified which fields are susceptible to multisensory influences. To reconcile findings from human imaging with anatomical knowledge from nonhuman primates, we exploited high-resolution imaging (functional magnetic resonance imaging) of the macaque monkey to study the modulation of auditory processing by visual stimulation. Using a functional parcellation of auditory cortex, we localized modulations to individual fields. Our results demonstrate that both primary (core) and nonprimary (belt) auditory fields can be activated by the mere presentation of visual scenes. Audiovisual convergence was restricted to caudal fields [prominently the core field (primary auditory cortex) and belt fields (caudomedial field, caudolateral field, and mediomedial field)] and continued in the auditory parabelt and the superior temporal sulcus. The same fields exhibited enhancement of auditory activation by visual stimulation and showed stronger enhancement for less effective stimuli, two characteristics of sensory integration. Together, these findings reveal multisensory modulation of auditory processing prominently in caudal fields but also at the lowest stages of auditory cortical processing.

Integration of Touch and Sound in Auditory Cortex

To form a coherent percept of the environment, our brain combines information from different senses. Such multisensory integration occurs in higher association cortices; but supposedly, it also occurs in early sensory areas. Confirming the latter hypothesis, we unequivocally demonstrate supra-additive integration of touch and sound stimulation at the second stage of the auditory cortex. Using high-resolution fMRI of the macaque monkey, we quantified the integration of auditory broad-band noise and tactile stimulation of hand and foot in anaesthetized animals. Integration was found posterior to and along the lateral side of the primary auditory cortex in the caudal auditory belt. Integration was stronger for temporally coincident stimuli and obeyed the principle of inverse effectiveness: greater enhancement for less effective stimuli. These findings demonstrates that multisensory integration occurs early and close to primary sensory areas and--because it occurs in anaesthetized animals--suggests that this integration is mediated by preattentive bottom-up mechanisms.

Sleep and Memory Consolidation: The Role of Electrophysiological Neuroimaging. Schlaf und Gedachtniskonsolidierung: Welchen Beitrag kann elektrophysiologisches Neuroimaging liefern?

Memory consolidation involves a complex series of molecular, cellular and network-level processes that take place on time scales from millisecond to months. Evidence from a wide range of experimental observations supports the hypothesis that parts of these processes occur during sleep when the brain is not engaged in processing and encoding incoming information. Indeed, sleep seems to be favorable for brain plasticity. Experience-dependent cortical plasticity observed during sleep has been hypothesized to be part of the global process of memory consolidation. Thus, studying task-dependent regionally specific reactivation of neuronal assemblies during posttraining sleep may make important contributions to elucidating the role of sleep in memory trace processing. A new methodology—low-resolution brain electromagnetic tomography (LORETA)—offers the possibility of localizing electrical activity produced by cortical neuronal generators under normal (undisturbed) sleeping conditions. The high time resolution of brain electrical data can be exploited to produce neuroimages for specific EEG spectral frequency bands (e.g. delta, theta, or spindle bands). This makes it possible to investigate, dependent on the type of memory, when—in which sleep stages (S2 sleep, SWS, REM sleep)—and where—in which cortical brain regions (primary sensory cortex, higher association cortex)—experience-dependent reactivation occurs.

A quantitative analysis of stimulus- and movement-related responses in the posterior parietal cortex of the monkey.

The posterior parietal cortex (areas 5 and 7) in monkeys has been described as a higher association cortex and as such, area 5 has been attributed a complex somaesthetic function. More recently, a role in the formation of motor commands has been postulated for these two cortical areas. We have been particularly interested in the role area 5 neurons may have in movement initiation. Single neuron activity was recorded in area 5 during the performance of a trained forelimb movement in monkeys and neuronal responses which occurred prior to movement were observed. In the present report, we have examined the neuronal discharge data trial by trial using a technique of data analysis which enabled us to separate the changes in neuronal activity into stimulus- or movement-related responses. Both stimulus- and movement-related responses were identified. The stimulus-related responses were not simple sensory responses since they were also influenced by the timing of the onset of movement. These results suggest that certain area 5 neurons may be involved in the linking of sensory inputs with motor outputs. Cerebrocerebellar loops may be a pathway in this linkage. The latencies of the movement-related responses were such that corollary discharge from the motor cortex may have played a role in this activity. Such corollary discharge may be a form of information used by the animal to execute movement in the absence of peripheral feedback.