Attention Samples Stimuli Rhythmically

When social animals communicate, the onset of informative content in one modality varies considerably relative to the other, such as when visual orofacial movements precede a vocalization. These naturally occurring asynchronies do not disrupt intelligibility or perceptual coherence. However, they occur on time scales where they likely affect integrative neuronal activity in ways that have remained unclear, especially for hierarchically downstream regions in which neurons exhibit temporally imprecise but highly selective responses to communication signals. To address this, we exploited naturally occurring face-and voice-onset asynchronies in primate vocalizations. Using these as stimuli we recorded cortical oscillations and neuronal spiking responses from functional MRI (fMRI)-localized voice-sensitive cortex in the anterior temporal lobe of macaques. We show that the onset of the visual face stimulus resets the phase of low-frequency oscillations, and that the face-voice asynchrony affects the prominence of two key types of neuronal multisensory responses: enhancement or suppression. Our findings show a three-way association between temporal delays in audiovisual communication signals, phase-resetting of ongoing oscillations, and the sign of multisensory responses. The results reveal how natural onset asynchronies in cross-sensory inputs regulate network oscillations and neuronal excitability in the voice-sensitive cortex of macaques, a suggested animal model for human voice areas. These findings also advance predictions on the impact of multisensory input on neuronal processes in face areas and other brain regions.H ow the brain parses multisensory input despite the variable and often large differences in the onset of sensory signals across different modalities remains unclear. We can maintain a coherent multisensory percept across a considerable range of spatial and temporal discrepancies (1-4): For example, auditory and visual speech signals can be perceived as belonging to the same multisensory "object" over temporal windows of hundreds of milliseconds (5-7). However, such misalignment can drastically affect neuronal responses in ways that may also differ between brain regions (8-10). We asked how natural asynchronies in the onset of face/voice content in communication signals would affect voice-sensitive cortex, a region in the ventral "object" pathway (11) where neurons (i) are selective for auditory features in communication sounds (12)(13)(14), (ii) are influenced by visual "face" content (12), and (iii) display relatively slow and temporally variable responses in comparison with neurons in primary auditory cortical or subcortical structures (14-16).Neurophysiological studies in human and nonhuman animals have provided considerable insights into the role of cortical oscillations during multisensory conditions and for parsing speech. Cortical oscillations entrain to the slow temporal dynamics of natural sounds (17)(18)(19)(20) and are thought to reflect the excitability of local networks to sensory inputs...

Section: Discussionmentioning

confidence: 79%

Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex

Perrodin

Kayser

Logothetis

et al. 2014

“…The RVF advantage might therefore result from degraded orthographic information transferred from the right hemisphere or, alternatively, from the left-right asymmetry of attention that has been a result of the Western reading style (31). A recent study investigating attentional capture with nonlinguistic stimuli supports the role of differential oscillatory sampling mechanisms for the two hemispheres (32).…”

Section: Split Visual Field Experimentsmentioning

confidence: 92%

Dynamic network structure of interhemispheric coordination

Doron

Bassett

Gazzaniga

2012

137

146

Fifty years ago Gazzaniga and coworkers published a seminal article that discussed the separate roles of the cerebral hemispheres in humans. Today, the study of interhemispheric communication is facilitated by a battery of novel data analysis techniques drawn from across disciplinary boundaries, including dynamic systems theory and network theory. These techniques enable the characterization of dynamic changes in the brain's functional connectivity, thereby providing an unprecedented means of decoding interhemispheric communication. Here, we illustrate the use of these techniques to examine interhemispheric coordination in healthy human participants performing a split visual field experiment in which they process lexical stimuli. We find that interhemispheric coordination is greater when lexical information is introduced to the right hemisphere and must subsequently be transferred to the left hemisphere for language processing than when it is directly introduced to the language-dominant (left) hemisphere. Further, we find that putative functional modules defined by coherent interhemispheric coordination come online in a transient manner, highlighting the underlying dynamic nature of brain communication. Our work illustrates that recently developed dynamic, network-based analysis techniques can provide novel and previously unapproachable insights into the role of interhemispheric coordination in cognition.T he field of split-brain research began several decades ago with the use of a drastic surgical solution for intractable epilepsy (1-3): the severing of the corpus callosum. This procedure significantly decreased the connectivity between the hemispheres, thereby irrevocably altering interhemispheric communication. Although a few interhemispheric pathways remained through subcortical structures and the anterior commissure, examination of callosal function using split visual field experiments clearly demonstrated its role in interhemispheric communication (2). The callosal projection plays a particularly crucial role in a variety of sensory-motor integrative functions of the two hemispheres (4), shows changes with age, and demonstrates the potential for dynamic changes with training (5). In fact, experiments in patients with severance of the callosum revealed that it subserves a large range of behaviors and cognitive functions that underlie the varied workings of the mind.Interhemispheric communication has been studied using two basic approaches. The first uses behavioral experiments to examine cognitive phenotypes, and the second uses neuroscientific experiments to examine brain phenotypes. Split-brain research initially focused on the former: Patients demonstrated striking behavioral phenotypes that provided clues regarding the underlying mechanics of brain communication. For example, although most perceptual processing appears to be isolated in each hemisphere following surgery, some attentional and emotional mechanisms initiated in one hemisphere can still be communicated to the other, cortically disconnected,...

“…An alternative explanation is that this activity is a component of an attentional process related to the anticipation of a novel stimulus, and that this anticipation is conducive to processes involved in memory storage (65). It was recently demonstrated that target detection performance fluctuates rhythmically within the theta-band frequency range (66), providing evidence that covert attentional processes, like some exploratory behaviors, are rhythmic in nature and possibly synchronize with oscillatory neural patterns.…”

Section: Discussionmentioning

confidence: 99%

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

Self Cite

253

266

Primates explore the visual world through the use of saccadic eye movements. Neuronal activity in the hippocampus, a structure known to be essential for memory, is modulated by this saccadic activity, but the relationship between visual exploration through saccades and memory formation is not well understood. Here, we identify a link between theta-band (3-12 Hz) oscillatory activity in the hippocampus and saccadic activity in monkeys performing a recognition memory task. As monkeys freely explored novel images, saccades produced a theta-band phase reset, and the reliability of this phase reset was predictive of subsequent recognition. In addition, enhanced theta-band power before stimulus onset predicted stronger stimulus encoding. Together, these data suggest that hippocampal theta-band oscillations act in concert with active exploration in the primate and possibly serve to establish the optimal conditions for stimulus encoding.T he use of saccadic eye movements to acquire information about the surrounding environment is perhaps the most conspicuous example of exploratory behavior in the primate. This behavior provides a mechanism for parsing incoming information into discrete, stable segments (i.e., snapshots of individual elements comprising a complex visual scene, allowing time for sufficient processing to occur before moving to the next fixation target). This mechanism of actively sampling sensory information from the environment may be similar to the behaviors engaged in by rodents exploring their environment through such activities as sniffing and whisking. Specifically, the fixation period following each saccade may be homologous to the period of incoming sensory information accompanying each sniff cycle in the rodent (1). Recently, it has been suggested that motor behaviors associated with information gathering are integral to the "active sensing" process in natural behavior (2). It is plausible that there may exist certain common neuronal elements across species that are associated with active sensing processes, such that the neuronal mechanisms underlying the encoding of information are intimately connected with the motor activities involved in acquiring that information.In many mammalian species, voluntary, exploratory behaviors are often associated with theta-band activity, a prominent 3-to 12-Hz oscillatory activity in the hippocampus and other limbic structures. This activity has been studied extensively in the rodent hippocampus (3-5), but it has also been described in bats (6), cats (7), and, more recently, humans (8-11). In rodents, theta appears to show close temporal relationships with running (3, 12) and sniffing (13), suggesting an association between theta and the rate of sensory input. Although hippocampal theta has been identified in anesthetized monkeys (14), the lack of a clear demonstration of hippocampal theta in awake monkeys has been attributed to the fact that the recording methods typically require immobile, head-affixed monkeys, in contrast to rodent studies using freely moving ...