Neural Synchrony in Attention and Consciousness

Lawrence M. WardUniversity of British Columbia

Funded by

Collaborators: Sam Doesburg, Kei Kitajo, Alexa Roggeveen, Tony Herdman, Jessica Green, John J. McDonald

Themes

Neural synchrony and its measurementNeural synchrony in attention: baton-passing in the cerebral cortexNeural synchrony in consciousness: binocular rivalry and the thalamic dynamic coreImplications for LIDA

Neural synchrony occurs when neural activity, spiking or dendritic currents,

in disparate locations rises and

falls in a fixed relationship

Gray & Singer’s cats

Ward et al’s humans

Varela et al, 2001

10 20 30 40 50

Frequency

Spectral

Power

Theta 6 Hz

10 20 30 40 50

Frequency

Spectral

Power

Gamma 40 Hz

10 20 30 40 50

Frequency

Spectral

Power

Alpha 10 Hz

Spectral power in a given frequency range reflects

local synchrony

Roles of local neural synchrony

High fidelity neural communicationPerceptual/memorial/motor…. Binding:

Increase 30-70 Hz: amplify post-synaptic effect by increasing spike co-occurrence (Fries et al, 2001)Decrease 6-15 Hz: increase post-synaptic impact by avoiding spike-frequency adaptation (Fries et al, 2001)

Fries 2005

Roles of global neural synchrony

Integration of neural activity through reciprocal (re-entrant) interactions between diverse brain regions (e.g., Varela et al, 2001)

Exchange of data (upward) and hypotheses/templates (downward); sensory/perceptual processingModulation of one region (e.g., hippocampus) by another (e.g., visual cortex) to store a memory (e.g., of a visual scene)Modulation of one region (e.g., visual cortex) by another (e.g., prefrontal cortex) to enhance processing of attended information (e.g., a sign for a sushi bar)Initiating an action in motor regions by computations from cognitive regionsConsciousness (?)

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phase 30Hz (C3, O1, Fz)

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Step.2 instantaneous phase and amplitude

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EEG/MEG synchronization analysis: calculation of phase locking value (PLV)

Step.1 Obtain SCD of filtered signals f(t) via bandpass filtering at chosen frequencies

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stimulus

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stimulus

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F7 F8

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Step.3 Calculation of phase locking value (PLV) for each time point

C3-O1

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O1-Fz(sec)

phase difference (30Hz)

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(400ms) period baseline in the PLV ofdeviation standard the:

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Step.4 standardization of PLV

Standardized PLV

(sec)

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To reduce the effect of volume conduction of stable sources and compare between electrode pairs at different distances

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Step.5 statistical test using surrogate data

Standardized PLV and surrogate PLV PLV (original)

±95 percentlePLVsurrogate

Median PLVsurrogate

(sec)

significant PLV increase

(Hz)60

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1009998

3-97210

sync

desync

Note: Local and long-range PLVz

must change together for

spurious synchronization to

be indicated (Doesburg,Ward,

CC, 2007)

Alpha, gamma and attention

Local alpha power associated with active suppressionLocal gamma power associated with active processingAlpha suppression necessary for gamma binding?Roles of long-range alpha and gamma synchrony?Coordination of local and long-range synchronization?Theta-modulated gamma synchrony

e.g., Klimesch, Jensen & Colgin, Palva & Palva, Ward

Doesburg, Roggeveen, Kitajo & Ward, 2007, Cerebral Cortex

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Left Cue 11 Hz

Right Cue 11 Hz

Left Cue 39 Hz

Right Cue 39 Hz

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Right Cue 11 Hz

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Right Cue 39 Hz

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P7 P8

P7 P8

Alpha/gamma local synchrony (power) indexes spatial attention orienting•Arrow cued box to attend to

•Press button only if + in attended box, not if x nor if in unattended box•Cue-target SOA 1000-1200 ms•Cue onset at 0 ms in figures

+

•At 250 ms (same as local power max gamma/min alpha) increase in global phase locking at diverse frequencies

•Lateralized in gamma band: P7 (left) for right target, P8 (right) for left target (orienting?)

•Increased synch in beta band also but not lateralized (readying?)

•Desynch at 100 ms in gamma: erasing old network?

QuickTime™ and a decompressor

are needed to see this picture.

Long-distance gamma synchrony establishes focused attention network

MEG replication

Increased lateralized synchronization in high alpha band from ~400 ms post cue onset until end of epochDecreased synchronization side ipsilateral to cueSynchronization in alpha band associated with maintenance of attentional focus at cued location

Doesburg, Ward, 2007, Proceedings BIOMAG2006

Left cue 14 Hz Right cue

What is SAM beamformer?

Synthetic Aperture Magnetometry (Vrba & Robinson 2001, Methods) Based on time/space covariance matrix of sensorsAchieves estimate of source power for each voxel in brain region from weighted linear combination of all measurements (where weights are selected to attenuate signals from all other voxels):

Optimal coefficients found by minimizing total power over time (computational tricks used in practice).

)()(ˆ ttS tmWθθ =

MEG Replication

MEG filtered at 14 HzSAM beamformer sources in parietal (SPL?) and visual cortices (n=5)PLV analysis applied to broadband source activity filtered from 6 Hz to 60 Hz14 Hz PLV shows lateralized increased synchrony similar to sensor analysis from 400-1000 ms post cue onset (right; n=2)40 Hz (gamma-band) PLV shows burst of lateralized increased synchrony at ~200-250 ms post cue onsetTheta rate gamma synch bursts at least for right parietal-occipital when attending leftDoesburg,Herdman, Ward, 2007, Cognitive Neuroscience Society

MEG replication

Beamformer sources projected to cortical surface (star=source in a sulcus so projection done by hand)Lateralized increases and decreases in synchrony between parietal and occipital sources in alpha band from 400-800 ms post cue onset (here 800 ms and 14 Hz)Occipital 14 Hz power replicates EEG data (blue bars, 800 ms)

Doesburg, Herdman, Ward, 2007, Cognitive Neuroscience Society

MEG Replication

Endogenous orienting: dorsal fronto- parietal (FEF, IPS, V1/V2)We also found FEF sources but not consistent enough for PLV analysisNot enough to activate relevant areas - must be synchronized to be functionally effective?

Corbetta and Shulman (2002) Nat Rev Neurosci; Wright & Ward, 2008, Orienting of Attention

EEG Replication: BESA beamformer sources from theta band signals

Green & McDonald, 2008, PLoS Biology

EEG analyses

BESA beamformer sources in theta band identifiedBroadband activity of dipoles at peak voxels computed based on EEG recordingsBroadband signals filtered and analytic signal, PLV etc., computed between sources

Lateralized increased synchronization in the alpha band

Doesburg, Green, Ward & McDonald, in prep.

350 ms post cue onset until target onset:

maintains attention at cued location

Left-neutral

Right-neutral

Right brain

Left brain

Baton-passing in the cerebral cortex

Auditory cues and targetsCue types: up or down glide for orient left or right (or vice versa), both for do not orient; each on 1/3 of trialsWhite noise targets (respond to all targets) for gap discrimination presented left (1/3 of trials) or right (1/3 of trials) at random regardless of cue type; probes (respond only if at cued location) presented on 1/3 of trials at randomBESA beamformer source analyses for theta-band signal

Green, Doesburg, Ward & McDonald, submitted

Valid Neutral

Invalid

RT 694 ms (25.5)

718 ms (26.6)

716 ms (26.7)

% Corr

90.9 (.016)

90.7 (.014)

90.6

(.018)

Theta-band BESA beamformer source activations

Baton-passing:

•1 Cue activates STG which in turn activates IPL and SPL

•2 IPL/SPL activate IFG

•3. IFG interprets cue

•4. IFG tells IPL/SPL where to orient

•5. IPL/SPL activate relevant STG and maintain activation until target

Green, Doesburg, Ward & McDonald, submitted

Interim Summary

Brain configured to attend to a specific location by

Confluence of burst of decreased local alpha power, increased local gamma power and increased long-range gamma synchrony at 250 ms post cueAttention maintained at specific location by increased long-range alpha-band synchrony (at least parietal-visual) that coincides with decreased local alpha powerInformation/control signals passed between brain regions by establishing and breaking synchronization in gamma band between those regions

Still not understood: mechanism of synchrony used (thalamic control?); nature of signals exchanged (control/compliance signals?); how reactivity of sensory cortex is increased by control signal; ……

Binocular rivalry: window to awareness

Stimuli

Apparent locus of fused object

Prisms

Eyes

Constant stimulation, involuntaril

y alternating experience

Corresponding retinal areas

Neural synchrony and consciousness

Cosmelli et al, (2004) Waves of consciousness: Ongoing cortical patterns during binocular rivalry. NeuroImage, 23,

128-140

Widespread 5 Hz synchrony associated with perception of the 5 Hz stimulus

Face Rings FaceFaceFace FaceRings Rings Rings

Synchrony of brain areas at 5 Hz for

different subjects; note individual

differences in both locations of active brain areas and in

amount of synchrony between them.

Binocular rivalry: window to awareness

Corresponding retinal areas

Stimuli

Apparent locus of fused object

Prisms

Eyes

Constant stimulation, involuntarily alternating experience; subjects press one of two buttons to indicate which pattern they see, neither to indicate parts of both

Long-range theta-rate bursts of gamma-band synchrony in binocular rivalry of striped patterns

Doesburg, Kitajo & Ward, 2005, NeuroReport

45Hz -450 -400 -350 -300 -250 -200 -150 -100 -50 0 50 100ms

7Hz -450 -400 -350 -300 -250 -200 -150 -100 -50 0 50 100ms

Button press at 0

Frequency (Hz)

Time (ms)

Time (ms – 0 indicates button press)

Fre

qu

en

cy

(H

z)R

L

BESA beamformer (280-220 ms pre-button-press, 36-46 Hz) applied to replication

Average PLVz over 8 active sources: R/L V1/V2, R sup occipital, R parietal, L temporal pole, L DLPF, R/L prefrontalBursts of gamma-band synchronization occur at theta rate (arrows) around button press in presence of persisting synchronization in theta band; also bursts of synchronization in beta band

Theta-modulated synchronizationLeft V1/V2 – Left DLPFC

surrogate level 0.025/0.025

Left V1/V2 – Right parietal

Right parietal – Right occipital

40-50 Hz synch

30-40 Hz synch

20-30 Hz synch40-50 Hz alt synch/desynch

40-50 Hz desynch

30-40 Hz desynch

Right brain

Left brain

Dynamic core hypothesis

Neural correlate of conscious awareness is what Tononi & Edelman called the "dynamic core"

Large-scale (brain-wide, 200-msec time scale)

Coherent (statistically synchronous) activity

Millions of neurons involved

Dynamic core hypothesis

DC simultaneously integrates activities of many brain areas (not all of them, a constantly changing subset) …And also differentiates current conscious state from many other, possible conscious states. My (radical) proposal: the thalamic dynamic core is the neural correlate of phenomenal awareness

Cortex computes, thalamus experiences Human cortex, with more neurons and more cortico-cortical fibers per thalamic fiber computes much more complex contents than do, e.g., rat, dog, or chimp cortices; pace Paul NunezCortical DC arises from synchronous activity in thalamus

Thalamic dynamic core

Dynamic core and supporting binocular rivalry data (Tononi & Edelman, Varela group); neural synchrony is keyLesions, neurosurgery, and anesthetic action point to thalamic “relay” nuclei as critical (Penfield, Alkire et al)Anatomy and function of thalamus and cortex (Mumford)We experience results (products) of computations, not the computations (processes) themselves (Lashley, Kinsbourne, Prinz, Rees, Koch, Baars)

Karen Ann Quinlan’s Brain at Autopsy (see Kinney et al 1994)

Thalamus-massive loss Cortex-little loss

Lesions: Karen Ann Quinlan

Drug/alcohol reaction; permanent vegetative state for 14 years

Penfield’s neurosurgery and stimulation mapping

Patient M.M.

treated for intractable epilepsy

M.M.’s cerebral cortex mapped via electrical stimulation by

Penfield

Neurosurgery and stimulation mapping

Penfield (The Mystery of the Mind, 1975):The mechanisms of epilepsy and electrical stimulation mapping imply that “…there are two brain mechanisms that have strategically placed gray matter in the diencephalon …, viz. (a) the mind’s mechanism (or highest brain mechanism); and (b) the computer (or automatic sensory-motor mechanism).” (p. 40).

Penfield’s “mind mechanism”

Merker (2006, BBS): argued SC is locus of

conscious analog simulation of world

General anesthesia

Alkire et al (2000) Consciousness & Cognition:

Common brain loci and mode of action of different general anesthetics imply that the critical mechanism of general anesthesia is a hyperpolarization block of the thalamic relay nuclei neurons

Alkire et al (2000) Consciousness & Cognition

Common brain areas where halothane and isoflurane anesthesia significantly depresses

activity; a. thalamus, b. midbrain reticular formation

The thalamus

Synchronizes cortical oscillations“Gateway” to cortex for major sensory systems (except smell)Evolved along with the cerebral cortex; a “seventh layer” of cortex (but with different neuron type)Each cortical area has an associated subnucleus of thalamus with massive cortico-thalamic projections and smaller thalamo-cortical projections; most thalamic subnuclei have no other inputs!

Where is the thalamus?

Thalamus

Pineal body

Gross Anatomy of some cortico-thalamic circuits

Roles of the thalamus

Relay station and gateway (attentional engagement) to cortex for sensory systemsSynchronizes neural activity in remote cortical areasActive blackboard that echoes back to cortex results of latest computations (Mumford)Site of dynamic core of neural activity that gives rise to phenomenal experience(?): thalamic dynamic core

We experience products…

Crovitz: maximum rate of consciously following strobe light = 4 to 5 Hz (250 to 200 msec per cycle) Sternberg STM scanning: no awareness of process; 40 Hz (25 ms/item) scan?LTM search & Retrieval: no awareness of memory search codes, only memoriesSpeech: not aware of composing utterences, phonemes, (co-)articulation, etc.

Conclusions

Synchronous neural oscillations occur at several scales and in particular frequency bandsLocal and global synchrony coordinate to establish an attentional network that enhances processing of attended stimuliNeural synchrony in the thalamo-cortical circuits, particularly in the thalamus, establishes a dynamic core of brain activity that supports (is?) conscious awareness

Implications for GWT/LIDA

Dynamic core is the GW GW (broadcasting) established by synchronization between various active processing modules mediated by thalamic dynamic core Transient networks of brain regions (processing coalitions) established by low frequency synchronization (carrier?), with high frequency synchronization establishing transient information exchange between processing areas in necessary temporal sequences (baton passing)Perception/action cycle governed by several temporal interactions based on processing speeds and communication requirements vis a vis available oscillation frequencies.