Daniel Senkowski

The multifaceted interplay between attention and multisensory integration

Multisensory integration has often been characterized as an automatic process. Recent findings indicate that multisensory integration can occur across various stages of stimulus processing that are linked to, and can be modulated by, attention. Stimulus-driven, bottom-up mechanisms induced by crossmodal interactions can automatically capture attention towards multisensory events, particularly when competition to focus elsewhere is relatively low. Conversely, top-down attention can facilitate the integration of multisensory inputs and lead to a spread of attention across sensory modalities. These findings point to a more intimate and multifaceted interplay between attention and multisensory integration than was previously thought. We review developments in the current understanding of the interactions between attention and multisensory processing, and propose a framework that unifies previous, apparently discordant, findings.

Crossmodal binding through neural coherence: implications for multisensory processing

Picture yourself on a crowded sideway with people milling about. The acoustic and visual signals generated by the crowd provide you with complementary information about their locations and motion which needs to be integrated. It is not well understood how such inputs from different sensory channels are combined into unified perceptual states. Coherence of oscillatory neural signals might be an essential mechanism supporting multisensory perception. Evidence is now emerging which indicates that coupled oscillatory activity might serve to link neural signals across uni- and multisensory regions and to express the degree of crossmodal matching of stimulus-related information. These results argue for a new view on multisensory processing which considers the dynamic interplay of neural populations as a key to crossmodal integration.

Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing

OBJECTIVE Integration of sensory information by cortical network binding appears to be crucially involved in target detection. Studies in schizophrenia using functional and diffusion tensor neuroimaging, event-related potentials and EEG coherence indicate an impairment of cortical network coupling in this disorder. Previous electrophysiological investigations in animals and humans suggested that gamma activity (oscillations at around 40 Hz) is essential for cortical network binding. Studies in medicated schizophrenia provide evidence for a reduced gamma activity in the context of auditory stimulus processing. This is the first investigation of oscillatory activations in the gamma-band in an auditory oddball paradigm in unmedicated schizophrenic patients. METHODS EEG gamma-band responses (GBRs) of 15 drug-free schizophrenic patients and 15 age- and gender-matched healthy controls were compared. A wavelet transform based on Morlet wavelets was employed for the calculation of oscillatory GBRs. RESULTS In response to standard stimuli, early evoked GBRs (20-100 ms), which are supposed to reflect auditory cortex activation, did not show significant group differences. However, schizophrenic patients showed reduced evoked GBRs in a late latency range (220-350 ms), particularly after target stimuli. This deficit occurred over right frontal scalp regions. Furthermore, significant correlations were observed between oscillatory GBRs and clinical parameters in schizophrenic patients. CONCLUSIONS The results are consistent with a relative preserved stimulus processing in the auditory cortex as reflected by the early GBR. The reduced late GBR is compatible with an abnormal interaction within a frontal lobe network, as was postulated by previous neuroimaging studies. SIGNIFICANCE The present study provides evidence for disturbed processing within frontal cortical regions in unmedicated schizophrenic patients as indicated by reduced evoked EEG GBRs.

Good times for multisensory integration: Effects of the precision of temporal synchrony as revealed by gamma-band oscillations

The synchronous occurrence of the unisensory components of a multisensory stimulus contributes to their successful merging into a coherent perceptual representation. Oscillatory gamma-band responses (GBRs, 30-80 Hz) have been linked to feature integration mechanisms and to multisensory processing, suggesting they may also be sensitive to the temporal alignment of multisensory stimulus components. Here we examined the effects on early oscillatory GBR brain activity of varying the precision of the temporal synchrony of the unisensory components of an audio-visual stimulus. Audio-visual stimuli were presented with stimulus onset asynchronies ranging from -125 to +125 ms. Randomized streams of auditory (A), visual (V), and audio-visual (AV) stimuli were presented centrally while subjects attended to either the auditory or visual modality to detect occasional targets. GBRs to auditory and visual components of multisensory AV stimuli were extracted for five subranges of asynchrony (e.g., A preceded by V by 100+/-25 ms, by 50+/-25 ms, etc.) and compared with GBRs to unisensory control stimuli. Robust multisensory interactions were observed in the early GBRs when the auditory and visual stimuli were presented with the closest synchrony. These effects were found over medial-frontal brain areas after 30-80 ms and over occipital brain areas after 60-120 ms. A second integration effect, possibly reflecting the perceptual separation of the two sensory inputs, was found over occipital areas when auditory inputs preceded visual by 100+/-25 ms. No significant interactions were observed for the other subranges of asynchrony. These results show that the precision of temporal synchrony can have an impact on early cross-modal interactions in human cortex.

Frontal and temporal dysfunction of auditory stimulus processing in schizophrenia.

Attention deficits have been consistently described in schizophrenia. Functional neuroimaging and electrophysiological studies have focused on anterior cingulate cortex (ACC) dysfunction as a possible mediator. However, recent basic research has suggested that the effect of attention is also observed as a relative amplification of activity in modality-associated cortical areas. In the present study, the question was addressed whether an amplification deficit is seen in the auditory cortex of schizophrenic patients during an attention-requiring choice reaction task. Twenty-one drug-free schizophrenic patients and 21 age- and sex-matched healthy controls were studied (32-channel EEG). The underlying generators of the event-related N1 component were separated in neuroanatomic space using a minimum-norm (LORETA) and a multiple dipole (BESA) approach. Both methods revealed activation in the primary auditory cortex (peak latency approximately 100 ms) and in the area of the ACC (peak latency approximately 130 ms). In addition, the adapted multiple dipole model also showed a temporal-radial source activation in nonprimary auditory areas (peak latency approximately 140 ms). In schizophrenic patients, significant activation deficits were found in the ACC as well as in the left nonprimary auditory areas that differentially correlated with negative and positive symptoms. The results suggest that (1) the source in the nonprimary auditory cortex is detected only with a multiple dipole approach and (2) that the N1 generators in the ACC and in the nonprimary auditory cortex are dysfunctional in schizophrenia. This would be in line with the notion that attention deficits in schizophrenia involve an extended cortical network.

Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task

OBJECTIVE The present study examined oscillatory brain activity of the EEG gamma band and event-related potentials (ERPs) with relation to the difficulty of a visual discrimination task. METHODS Three tasks with identical stimulus material were performed by 9 healthy subjects. The tasks comprised a passive control task, and an easy and a hard visual discrimination task, requiring discrimination of the color of circles. EEG was recorded from 26 electrodes. A wavelet transform based on Morlet wavelets was employed for the analysis of gamma activity. RESULTS Evoked EEG gamma activity was enhanced by both discrimination tasks as compared to the passive control task. Within the two discrimination tasks, the latency of the evoked gamma peak was delayed for the harder task. Higher amplitudes of the ERP components N170 and P300 were found in both discrimination tasks as compared to the passive task. The N2b, which showed a maximum activation at about 260 ms, was increased in the hard discrimination task as compared to the easy discrimination task. CONCLUSIONS Our results indicate that early evoked gamma activity and N2b are related to the difficulty of visual discrimination processes. A delayed gamma activity in the hard task indicated a longer duration of stimulus processing, whereas the amplitude of the N2b directly indicates the level of task difficulty.

Multisensory interactions in early evoked brain activity follow the principle of inverse effectiveness

A major determinant of multisensory integration, derived from single-neuron studies in animals, is the principle of inverse effectiveness (IE), which describes the phenomenon whereby maximal multisensory response enhancements occur when the constituent unisensory stimuli are minimally effective in evoking responses. Human behavioral studies, which have shown that multisensory interactions are strongest when stimuli are low in intensity are in agreement with the IE principle, but the neurophysiologic basis for this finding is unknown. In this high-density electroencephalography (EEG) study, we examined effects of stimulus intensity on multisensory audiovisual processing in event-related potentials (ERPs) and response time (RT) facilitation in the bisensory redundant target effect (RTE). The RTE describes that RTs are faster for bisensory redundant targets than for the respective unisensory targets. Participants were presented with semantically meaningless unisensory auditory, unisensory visual and bisensory audiovisual stimuli of low, middle and high intensity, while they were instructed to make a speeded button response when a stimulus in either modality was presented. Behavioral data showed that the RTE exceeded predictions on the basis of probability summations of unisensory RTs, indicative of integrative multisensory processing, but only for low intensity stimuli. Paralleling this finding, multisensory interactions in short latency (40-60ms) ERPs with a left posterior and right anterior topography were found particularly for stimuli with low intensity. Our findings demonstrate that the IE principle is applicable to early multisensory processing in humans.

Phase-Locking and Amplitude Modulations of EEG Alpha: Two Measures Reflect Different Cognitive Processes in a Working Memory Task

It has been demonstrated in numerous experiments that oscillatory EEG responses in the alpha frequency band (8-12 Hz) increase with memory load during the retention interval in working memory tasks. However, the findings diverge with respect to which measurement of alpha activity is influenced by memory processes. Here, we differentiate between evoked and total alpha activity in order to separate effects of phase-locking and amplitude modulation. We present data from a delayed-matching-to-sample task (S1-S2 paradigm) for which we compared EEG alpha responses between a perception and a memory condition. Increased total alpha activity was found in the retention interval for the memory as compared to the perception condition. Evoked alpha activity, however, did not differentiate between memory and perception conditions but, instead, was increased for the more complex condition of processing non-Kanizsa figures as compared to Kanizsa figures. Thus, our results demonstrate a functional differentiation between evoked and total alpha activity. While alpha phase locking seemed to be influenced mainly by task complexity, alpha amplitude clearly reflected memory demands in our paradigm.

Allelic variants of the functional promoter polymorphism of the human serotonin transporter gene is associated with auditory cortical stimulus processing.

The loudness dependence (LD) of the auditory-evoked N1/P2 component has been shown to be related to the central serotonergic neurotransmission. Allelic variants in the promoter region of the 5-hydroxytryptamine transporter (5-HTT) gene were shown to modulate serotonergic activity. It was hypothesized that the three genotypes (l/l, s/l, s/s) differ with respect to LD. Allelic variants of the 5-HTT promoter region and LD at the Cz electrode were determined in 185 healthy subjects prospectively. A significant association was found between LD and genotype (ANOVA: F=4.172, p=0.017). Individuals homozygous for the l allele exhibited a weaker LD compared to heterozygous subjects. The results are consistent with the reported association between 5-HTT genotype and serotonin transport capacity in lymphoblasts, and indicate that auditory stimulus processing is associated with genetic variants of the brain serotonergic system. The LD may serve as endophenotype in human serotonin research.

Evidence for disturbed cortical signal processing and altered serotonergic neurotransmission in generalized anxiety disorder

BACKGROUND Current pathophysiological concepts of generalized anxiety disorder (GAD) assume a disturbed exteroceptive sensory system. Furthermore, central serotonergic neurotransmission has been shown to play an important role in anxiety disorder. Cortical signal processing as measured by auditory evoked potentials (AEPs) may reflect the integrity of the exteroceptive sensory system. Because a special aspect of AEP, the loudness dependence of the N1/P2-component (LD), has been related to central serotonergic activity, the LD may be useful for investigating serotonergic dysfunctions in GAD. METHODS The LD was recorded in 31 medication-free patients with GAD without any psychiatric co-morbidity and in 31 matched control subjects. Dipole source analysis was performed to separate the LD of regions including the primary (LD-tangential dipole) and regions including the secondary auditory cortex (LD-radial dipole). RESULTS A shallower LD-tangential was observed in patients with GAD as compared to healthy control subjects [F(1,60) = 6.727, p =.012; one-way analysis of variance]. The LD-radial showed no differences between groups. Severity of the anxiety symptoms was not related to the LDs. CONCLUSIONS The results indicate an altered exteroceptive sensory system in GAD occurring at the level of the primary but not secondary auditory cortex. Because a shallow LD of the primary auditory cortex was related to a high firing rate of neurons in the dorsal raphe nucleus, the results may support evidence for an enhanced serotonergic activity in GAD.