The multisensory function of the human primary visual cortex

It has been nearly 10 years since Ghazanfar and Schroeder (2006) proposed that the neocortex is essentially multisensory in nature. However, it is only recently that sufficient and hard evidence that supports this proposal has accrued. We review evidence that activity within the human primary visual cortex plays an active role in multisensory processes and directly impacts behavioural outcome. This evidence emerges from a full pallet of human brain imaging and brain mapping methods with which multisensory processes are quantitatively assessed by taking advantage of particular strengths of each technique as well as advances in signal analyses. Several general conclusions about multisensory processes in primary visual cortex of humans are supported relatively solidly. First, haemodynamic methods (fMRI/PET) show that there is both convergence and integration occurring within primary visual cortex. Second, primary visual cortex is involved in multisensory processes during early post-stimulus stages (as revealed by EEG/ERP/ERFs as well as TMS). Third, multisensory effects in primary visual cortex directly impact behaviour and perception, as revealed by correlational (EEG/ERPs/ERFs) as well as more causal measures (TMS/tACS). While the provocative claim of Ghazanfar and Schroeder (2006) that the whole of neocortex is multisensory in function has yet to be demonstrated, this can now be considered established in the case of the human primary visual cortex

Selective attention to sound features mediates cross-modal activation of visual cortices.

Contemporary schemas of brain organization now include multisensory processes both in low-level cortices as well as at early stages of stimulus processing. Evidence has also accumulated showing that unisensory stimulus processing can result in cross-modal effects. For example, task-irrelevant and lateralised sounds can activate visual cortices; a phenomenon referred to as the auditory-evoked contralateral occipital positivity (ACOP). Some claim this is an example of automatic attentional capture in visual cortices. Other results, however, indicate that context may play a determinant role. Here, we investigated whether selective attention to spatial features of sounds is a determining factor in eliciting the ACOP. We recorded high-density auditory evoked potentials (AEPs) while participants selectively attended and discriminated sounds according to four possible stimulus attributes: location, pitch, speaker identity or syllable. Sound acoustics were held constant, and their location was always equiprobable (50% left, 50% right). The only manipulation was to which sound dimension participants attended. We analysed the AEP data from healthy participants within an electrical neuroimaging framework. The presence of sound-elicited activations of visual cortices depended on the to-be-discriminated, goal-based dimension. The ACOP was elicited only when participants were required to discriminate sound location, but not when they attended to any of the non-spatial features. These results provide a further indication that the ACOP is not automatic. Moreover, our findings showcase the interplay between task-relevance and spatial (un)predictability in determining the presence of the cross-modal activation of visual cortices

Early cross-modal interactions and adult human visual cortical plasticity revealed by binocular rivalry

In this research binocular rivalry is used as a tool to investigate different aspects of visual and multisensory perception. Several experiments presented here demonstrated that touch specifically interacts with vision during binocular rivalry and that the interaction likely occurs at early stages of visual processing, probably V1 or V2. Another line of research also presented here demonstrated that human adult visual cortex retains an unexpected high degree of experience-dependent plasticity by showing that a brief period of monocular deprivation produced important perceptual consequences on the dynamics of binocular rivalry, reflecting a homeostatic plasticity. In summary, this work shows that binocular rivalry is a powerful tool to investigate different aspects of visual perception and can be used to reveal unexpected properties of early visual cortex

Sensory dominance and multisensory integration as screening tools in aging

Multisensory information typically confers neural and behavioural advantages over unisensory information. We used a simple audio-visual detection task to compare healthy young (HY), healthy older (HO) and mild-cognitive impairment (MCI) individuals. Neuropsychological tests assessed individuals' learning and memory impairments. First, we provide much-needed clarification regarding the presence of enhanced multisensory benefits in both healthily and abnormally aging individuals. The pattern of sensory dominance shifted with healthy and abnormal aging to favour a propensity of auditory-dominant behaviour (i.e., detecting sounds faster than flashes). Notably, multisensory benefits were larger only in healthy older than younger individuals who were also visually-dominant. Second, we demonstrate that the multisensory detection task offers benefits as a time- and resource-economic MCI screening tool. Receiver operating characteristic (ROC) analysis demonstrated that MCI diagnosis could be reliably achieved based on the combination of indices of multisensory integration together with indices of sensory dominance. Our findings showcase the importance of sensory profiles in determining multisensory benefits in healthy and abnormal aging. Crucially, our findings open an exciting possibility for multisensory detection tasks to be used as a cost-effective screening tool. These findings clarify relationships between multisensory and memory functions in aging, while offering new avenues for improved dementia diagnostics

The COGs (context, object, and goals) in multisensory processing

Our understanding of how perception operates in real-world environments has been substantially advanced by studying both multisensory processes and “top-down” control processes influencing sensory processing via activity from higher-order brain areas, such as attention, memory, and expectations. As the two topics have been traditionally studied separately, the mechanisms orchestrating real-world multisensory processing remain unclear. Past work has revealed that the observer’s goals gate the influence of many multisensory processes on brain and behavioural responses, whereas some other multisensory processes might occur independently of these goals. Consequently, other forms of top-down control beyond goal dependence are necessary to explain the full range of multisensory effects currently reported at the brain and the cognitive level. These forms of control include sensitivity to stimulus context as well as the detection of matches (or lack thereof) between a multisensory stimulus and categorical attributes of naturalistic objects (e.g. tools, animals). In this review we discuss and integrate the existing findings that demonstrate the importance of such goal-, object- and context-based top-down control over multisensory processing. We then put forward a few principles emerging from this literature review with respect to the mechanisms underlying multisensory processing and discuss their possible broader implications

Sounds enhance visual completion processes.

Everyday vision includes the detection of stimuli, figure-ground segregation, as well as object localization and recognition. Such processes must often surmount impoverished or noisy conditions; borders are perceived despite occlusion or absent contrast gradients. These illusory contours (ICs) are an example of so-called mid-level vision, with an event-related potential (ERP) correlate at ∼100-150 ms post-stimulus onset and originating within lateral-occipital cortices (the IC <sub>effect</sub> ). Presently, visual completion processes supporting IC perception are considered exclusively visual; any influence from other sensory modalities is currently unknown. It is now well-established that multisensory processes can influence both low-level vision (e.g. detection) as well as higher-level object recognition. By contrast, it is unknown if mid-level vision exhibits multisensory benefits and, if so, through what mechanisms. We hypothesized that sounds would impact the IC <sub>effect</sub> . We recorded 128-channel ERPs from 17 healthy, sighted participants who viewed ICs or no-contour (NC) counterparts either in the presence or absence of task-irrelevant sounds. The IC <sub>effect</sub> was enhanced by sounds and resulted in the recruitment of a distinct configuration of active brain areas over the 70-170 ms post-stimulus period. IC-related source-level activity within the lateral occipital cortex (LOC), inferior parietal lobe (IPL), as well as primary visual cortex (V1) were enhanced by sounds. Moreover, the activity in these regions was correlated when sounds were present, but not when absent. Results from a control experiment, which employed amodal variants of the stimuli, suggested that sounds impact the perceived brightness of the IC rather than shape formation per se. We provide the first demonstration that multisensory processes augment mid-level vision and everyday visual completion processes, and that one of the mechanisms is brightness enhancement. These results have important implications for the design of treatments and/or visual aids for low-vision patients

On the role of neuronal oscillations in auditory cortical processing

Although it has been over 100 years since William James stated that everyone knows what attention is , its underlying neural mechanisms are still being debated today. The goal of this research was to describe the physiological mechanisms of auditory attention using direct electrophysiological recordings in macaque primary auditory cortex (A1). A major focus of my research was on the role ongoing neuronal oscillations play in attentional modulation of auditory responses in A1. For all studies, laminar profiles of synaptic activity, (indexed by current source density analysis) and concomitant firing patterns in local neurons (multiunit activity) were acquired simultaneously via linear array multielectrodes positioned in A1. The initial study of this dissertation examined the contribution of ongoing oscillatory activity to excitatory and inhibitory responses in A1 in passive (no task) conditions. Next, the function of ongoing oscillations in modulating the frequency tuning of A1 during an intermodal selective attention oddball task was investigated. The last study was aimed at establishing whether there is a hemispheric asymmetry in the way neuronal oscillations are utilized by attention, corresponding to that noted in humans. The results of the first study indicate that in passive conditions, ongoing oscillations reset by stimulus related inputs modulate both excitatory and inhibitory components of local neuronal ensemble responses in A1. The second set of experiments demonstrates that this mechanism is utilized by attention to modulate and sharpen frequency tuning. Finally, we show that as in humans, there appears to be a specialization of left A1 for temporal processing, as signified by greater temporal precision of neuronal oscillatory alignment. Taken together these results underline the importance of neuronal oscillations in perceptual processes, and the validity of the macaque monkey as a model of human auditory processing

Neural oscillatory signatures of auditory and audiovisual illusions

Questions of the relationship between human perception and brain activity can be approached from different perspectives: in the first, the brain is mainly regarded as a recipient and processor of sensory data. The corresponding research objective is to establish mappings of neural activity patterns and external stimuli. Alternatively, the brain can be regarded as a self-organized dynamical system, whose constantly changing state affects how incoming sensory signals are processed and perceived. The research reported in this thesis can chiefly be located in the second framework, and investigates the relationship between oscillatory brain activity and the perception of ambiguous stimuli. Oscillations are here considered as a mechanism for the formation of transient neural assemblies, which allows efficient information transfer. While the relevance of activity in distinct frequency bands for auditory and audiovisual perception is well established, different functional architectures of sensory integration can be derived from the literature. This dissertation therefore aims to further clarify the role of oscillatory activity in the integration of sensory signals towards unified perceptual objects, using illusion paradigms as tools of study. In study 1, we investigate the role of low frequency power modulations and phase alignment in auditory object formation. We provide evidence that auditory restoration is associated with a power reduction, while the registration of an additional object is reflected by an increase in phase locking. In study 2, we analyze oscillatory power as a predictor of auditory influence on visual perception in the sound-induced flash illusion. We find that increased beta-/ gamma-band power over occipitotemporal electrodes shortly before stimulus onset predicts the illusion, suggesting a facilitation of processing in polymodal circuits. In study 3, we address the question of whether visual influence on auditory perception in the ventriloquist illusion is reflected in primary sensory or higher-order areas. We establish an association between reduced theta-band power in mediofrontal areas and the occurrence of illusion, which indicates a top-down influence on sensory decision-making. These findings broaden our understanding of the functional relevance of neural oscillations by showing that different processing modes, which are reflected in specific spatiotemporal activity patterns, operate in different instances of sensory integration.Fragen nach dem Zusammenhang zwischen menschlicher Wahrnehmung und Hirnaktivität können aus verschiedenen Perspektiven adressiert werden: in der einen wird das Gehirn hauptsächlich als Empfänger und Verarbeiter von sensorischen Daten angesehen. Das entsprechende Forschungsziel wäre eine Zuordnung von neuronalen Aktivitätsmustern zu externen Reizen. Dieser Sichtweise gegenüber steht ein Ansatz, der das Gehirn als selbstorganisiertes dynamisches System begreift, dessen sich ständig verändernder Zustand die Verarbeitung und Wahrnehmung von sensorischen Signalen beeinflusst. Die Arbeiten, die in dieser Dissertation zusammengefasst sind, können vor allem in der zweitgenannten Forschungsrichtung verortet werden, und untersuchen den Zusammenhang zwischen oszillatorischer Hirnaktivität und der Wahrnehmung von mehrdeutigen Stimuli. Oszillationen werden hier als ein Mechanismus für die Formation von transienten neuronalen Zusammenschlüssen angesehen, der effizienten Informationstransfer ermöglicht. Obwohl die Relevanz von Aktivität in verschiedenen Frequenzbändern für auditorische und audiovisuelle Wahrnehmung gut belegt ist, können verschiedene funktionelle Architekturen der sensorischen Integration aus der Literatur abgeleitet werden. Das Ziel dieser Dissertation ist deshalb eine Präzisierung der Rolle oszillatorischer Aktivität bei der Integration von sensorischen Signalen zu einheitlichen Wahrnehmungsobjekten mittels der Nutzung von Illusionsparadigmen. In der ersten Studie untersuchen wir die Rolle von Leistung und Phasenanpassung in niedrigen Frequenzbändern bei der Formation von auditorischen Objekten. Wir zeigen, dass die Wiederherstellung von Tönen mit einer Reduktion der Leistung zusammenhängt, während die Registrierung eines zusätzlichen Objekts durch einen erhöhten Phasenangleich widergespiegelt wird. In der zweiten Studie analysieren wir oszillatorische Leistung als Prädiktor von auditorischem Einfluss auf visuelle Wahrnehmung in der sound-induced flash illusion. Wir stellen fest, dass erhöhte Beta-/Gamma-Band Leistung über occipitotemporalen Elektroden kurz vor der Reizdarbietung das Auftreten der Illusion vorhersagt, was auf eine Begünstigung der Verarbeitung in polymodalen Arealen hinweist. In der dritten Studie widmen wir uns der Frage, ob ein visueller Einfluss auf auditorische Wahrnehmung in der ventriloquist illusion sich in primären sensorischen oder übergeordneten Arealen widerspiegelt. Wir weisen einen Zusammenhang von reduzierter Theta-Band Leistung in mediofrontalen Arealen und dem Auftreten der Illusion nach, was einen top-down Einfluss auf sensorische Entscheidungsprozesse anzeigt. Diese Befunde erweitern unser Verständnis der funktionellen Bedeutung neuronaler Oszillationen, indem sie aufzeigen, dass verschiedene Verarbeitungsmodi, die sich in spezifischen räumlich-zeitlichen Aktivitätsmustern spiegeln, in verschiedenen Phänomenen von sensorischer Integration wirksam sind