Jessica J. Green

Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics Mediating Visual Perception

Consciousness has been proposed to emerge from functionally integrated large-scale ensembles of gamma-synchronous neural populations that form and dissolve at a frequency in the theta band. We propose that discrete moments of perceptual experience are implemented by transient gamma-band synchronization of relevant cortical regions, and that disintegration and reintegration of these assemblies is time-locked to ongoing theta oscillations. In support of this hypothesis we provide evidence that (1) perceptual switching during binocular rivalry is time-locked to gamma-band synchronizations which recur at a theta rate, indicating that the onset of new conscious percepts coincides with the emergence of a new gamma-synchronous assembly that is locked to an ongoing theta rhythm; (2) localization of the generators of these gamma rhythms reveals recurrent prefrontal and parietal sources; (3) theta modulation of gamma-band synchronization is observed between and within the activated brain regions. These results suggest that ongoing theta-modulated-gamma mechanisms periodically reintegrate a large-scale prefrontal-parietal network critical for perceptual experience. Moreover, activation and network inclusion of inferior temporal cortex and motor cortex uniquely occurs on the cycle immediately preceding responses signaling perceptual switching. This suggests that the essential prefrontal-parietal oscillatory network is expanded to include additional cortical regions relevant to tasks and perceptions furnishing consciousness at that moment, in this case image processing and response initiation, and that these activations occur within a time frame consistent with the notion that conscious processes directly affect behaviour.

Electrical Neuroimaging Reveals Timing of Attentional Control Activity in Human Brain

Voluntarily shifting attention to a location of the visual field improves the perception of events that occur there. Regions of frontal cortex are thought to provide the top-down control signal that initiates a shift of attention, but because of the temporal limitations of functional brain imaging, the timing and sequence of attentional-control operations remain unknown. We used a new analytical technique (beamformer spatial filtering) to reconstruct the anatomical sources of low-frequency brain waves in humans associated with attentional control across time. Following a signal to shift attention, control activity was seen in parietal cortex 100–200 ms before activity was seen in frontal cortex. Parietal cortex was then reactivated prior to anticipatory biasing of activity in occipital cortex. The magnitudes of early parietal activations were strongly predictive of the degree of attentional improvement in perceptual performance. These results show that parietal cortex, not frontal cortex, provides the initial signals to shift attention and indicate that top-down attentional control is not purely top down.

From local inhibition to long-range integration: a functional dissociation of alpha-band synchronization across cortical scales in visuospatial attention.

When attention is allocated to one visual hemifield, increased alpha power is observed in ipsilateral visual cortex. This has been attributed to synchronization of alpha-band oscillations within cortical regions which reflects inhibitory processing. Recent results, however, indicate that synchronization of alpha oscillations between cortical regions is relevant for transient functional coupling. Such coupling is thought to be involved in orienting attention to a specific region of the visual field. We thus hypothesized that alpha-band synchronization between low-level visual cortex and higher-level visual brain regions would be increased in the hemisphere contralateral to an attended location. To test this hypothesis we calculated phase synchronization between attention-related EEG source activations occurring between predictive directional cues and expected visual targets. Alpha amplitude (understood as an index of local synchronization) within low-level visual cortex was increased ipsilateral to attended locations and decreased contralateral to attended locations, consistent with alpha-band scalp topography and previous research relating local alpha power to active inhibition. Increased long-range alpha-band synchronization between low-level visual cortex and parietal cortex, however, was observed contralateral to the attended visual hemifield, whereas decreased synchronization (phase scattering) was observed in the ipsilateral hemisphere. These results identify a potential mechanism for the enhanced processing of stimuli appearing at attended locations, as long-range synchronization is thought to increase the fidelity and effectiveness of communication between brain areas. Our observation of inhibitory amplitude changes, interpreted as increased local-area synchronization, and facilitatory long-range synchronization demonstrates a functional dissociation for alpha-band synchronization across cortical scales.

Lateralized frontal activity elicited by attention-directing visual and auditory cues

In event-related potential studies of voluntary spatial attention, lateralized activity observed over anterior scalp sites prior to an impending target has been interpreted as the activity of a supramodal attentional control mechanism in the frontal lobes. However, variability in the scalp topography and presence of this activity across studies suggests that multiple neural generators contribute to the lateralized activity recorded at the scalp. Using distributed source modeling we found two distinct frontal lobe sources following attention-directing cues, one dependent on the sensory modality of the eliciting stimulus and one dependent on the response requirements of the task. Differential activity of these sources depending on task parameters suggests that neither source reflects activity necessary for controlling attention.

Control mechanisms mediating shifts of attention in auditory and visual space: a spatio-temporal ERP analysis

The neural systems that mediate voluntary shifts of attention to visual and auditory stimuli were investigated by examining the patterns of human brain electricity elicited by attention-directing cues in auditory and visual tasks. Several lateralized event-related potential (ERP) components were observed when participants shifted attention in expectation of visual targets (experiment 1). One component was focused over frontal cortex and a second was focused primarily over the occipital-temporal cortex but also spread to parietal regions of the scalp. Previous work has indicated that the frontal component reflects supramodal processes involved in the executive control of attention and that the posterior component reflects either spatial attentional control processes in the posterior parietal lobe or modulation of processes in visual cortex. Here, the posterior component was observed when participants shifted attention in expectation of auditory targets (experiments 2–4), but the frontal component was found only in the visual task. The posterior component seemed to be generated in parietal and occipital areas even when there was no visual information about the to-be-attended locations. These results are consistent with the view that voluntary shifts of attention are mediated by supramodal processes in the parietal lobe and that the spatial coordinates of the to-be-attended location are based on visual representations of space.

On the Electrophysiological Evidence for the Capture of Visual Attention.

The presence of a salient distractor interferes with visual search. According to the salience-driven selection hypothesis, this interference is because of an initial deployment of attention to the distractor. Three event-related potential (ERP) findings have been regarded as evidence for this hypothesis: (a) salient distractors were found to elicit an ERP component called N2pc, which reflects attentional selection; (b) with target and distractor on opposite sides, a distractor N2pc was reported to precede the target N2pc (N2pc flip); (c) the distractor N2pc on slow-response trials was reported to occur particularly early, suggesting that the fastest shifts of attention were driven by salience. This evidence is equivocal, however, because the ERPs were noisy (b, c) and were averaged across all trials, thereby making it difficult to know whether attention was deployed directly to the target on some trials (a, b). We reevaluated this evidence using a larger sample size to reduce noise and by analyzing ERPs separately for fast- and slow-response trials. On fast-response trials, the distractor elicited a contralateral positivity (PD)-an index of attentional suppression-instead of an N2pc. There was no N2pc flip or early distractor N2pc. As it stands, then, there is no ERP evidence for the salience-driven selection hypothesis.

Electrical Neuroimaging of Voluntary Audiospatial Attention: Evidence for a Supramodal Attention Control Network

Previous attempts to investigate the supramodal nature of attentional control have focused primarily on identifying neuroanatomical overlap in the frontoparietal systems activated during voluntary shifts of spatial attention in different sensory modalities. However, the activation of the same neural structures is insufficient evidence for a supramodal system, as the same brain regions could interact with one another in very different ways during shifts of attention in different modalities. Thus, to explore the similarity of the functional networks, it is necessary to identify the neural structures involved and to examine the timing and sequence of activities within the network. To this end, we used an electrical neuroimaging technique to localize the neural sources of electroencephalographic signals recorded from human subjects during audiospatial shifts of attention and to examine the timing and sequence of activities within several regions of interest. We then compared the results to an analogous study of visuospatial attention shifts. Similar frontal and parietal regions were activated during visual and auditory shifts of attention, and the timing of activities within these regions was nearly identical. Following this modality-independent sequence of attention-control activity, activity in the relevant sensory cortex was enhanced in anticipation of the response-relevant target. These results are consistent with the hypothesis that a single supramodal network of frontal and parietal regions mediates voluntary shifts of spatial attention and controls the flow of sensory information in modality-specific sensory pathways.

Theta modulation of inter-regional gamma synchronization during auditory attention control.

Synchronization of gamma oscillations among brain regions is relevant for dynamically organizing communication among neurons to support cognitive and perceptual processing, including attention orienting. Recent research has demonstrated that inter-regional synchronization in the gamma-band is modulated by theta rhythms during cortical processing. It has been proposed that such cross-frequency dynamics underlie the integration of local processes into large-scale functional networks. To investigate the potential role of theta-gamma mechanisms during auditory attention control, we localized activated regions using EEG beamformer analysis, and calculated inter-regional gamma-band synchronization between activated regions as well as modulation of inter-regional gamma-band synchronization by the phase of cortical theta rhythms. Abundant synchronization of gamma-band oscillations among regions comprising the auditory attention control network was observed. This inter-regional gamma synchronization was modulated by theta phase. These results provide further evidence implicating inter-regional gamma-band synchronization, and theta-gamma interactions, in task-dependent communication among cortical regions, and provide the first evidence that such mechanisms are relevant for auditory attention control.

Isolating event-related potential components associated with voluntary control of visuo-spatial attention

Attention-directing cues presented at fixation evoke several lateralized event-related potential (ERP) components prior to the onset of visual targets. These components have been associated with the control of visuo-spatial attention, but the neuro-cognitive operations and neural generators of the components are still largely unknown. Here, we isolated cue-elicited ERP activity in different ways to home in on different neuro-cognitive operations and to gain a better understanding about the possible neuroanatomical sources of the cue-elicited ERP activities. To isolate lateralized cue-ERP activity, we compared shift-left and shift-right cue ERPs to shift-up cue ERPs. To measure all of the ERP activity related to attentional control, including spatially nonspecific activity that is removed in the process of isolating lateralized cue-ERP components, we compared shift-cue ERPs to neutral-cue (i.e., no-shift) ERPs. Isolated lateralized-ERP activity was seen in the contralateral-occipital lobe in the early phase of the cue-target interval and in the ipsilateral-occipital lobe in the late phase. The later, ipsilateral activity indicates that the late directing attention positivity (LDAP) reflected processing of the to-be-ignored location. The neutral-cue isolation revealed a shift-related positivity over posterior scalp regions and a shift-related negativity over more anterior scalp regions. The spatio-temporal sequence of shift-related activity observed on the scalp, together with estimates of distributed source activity underlying the shift-related ERP components, indicated that frontal and parietal regions of cortex participated in the control of attention and led to pre-target biasing in visual cortical areas.

The role of temporal predictability in the anticipatory biasing of sensory cortex during visuospatial shifts of attention

The presentation of an attention-directing cue elicits a lateralized ERP deflection called the late directing attention positivity (LDAP) and lateralized changes in alpha-band elelctroencephalogram oscillations. Both of these electrophysiological responses have been independently linked to biasing of visual cortex in anticipation of an impending target. However, the LDAP is not always observed, and the link between the ERP and alpha-band modulations remains unclear. Here, we examined the effect of advance knowledge of the time of target onset on the ERP and alpha-band responses to cues. The LDAP was present only when the attention-directing cues accurately indicated the time of target appearance, whereas two sequential attention-related alpha-band modulations were observed regardless of the temporal information provided by the cues. Thus, alpha-band activity may be a more reliable index of pretarget biasing of visual cortical activity than lateralized ERP effects.