Rhythms for Cognition: Communication through Coherence

Abstract

I propose that synchronization affects communication between neuronal groups. Gamma-band (30-90 Hz) synchronization modulates excitation rapidly enough that it escapes the following inhibition and activates postsynaptic neurons effectively. Synchronization also ensures that a presynaptic activation pattern arrives at postsynaptic neurons in a temporally coordinated manner. At a postsynaptic neuron, multiple presynaptic groups converge, e.g., representing different stimuli. If a stimulus is selected by attention, its neuronal representation shows stronger and higher-frequency gamma-band synchronization. Thereby, the attended stimulus representation selectively entrains postsynaptic neurons. The entrainment creates sequences of short excitation and longer inhibition that are coordinated between pre- and postsynaptic groups to transmit the attended representation and shut out competing inputs. The predominantly bottom-up-directed gamma-band influences are controlled by predominantly top-down-directed alpha-beta-band (8-20 Hz) influences. Attention itself samples stimuli at a 7-8 Hz theta rhythm. Thus, several rhythms and their interplay render neuronal communication effective, precise, and selective.

Copyright © 2015 Elsevier Inc. All rights reserved.

Figures

Figure 1. Natural viewing induces a gamma-band rhythm in visual cortex

Raw LFP trace recorded as the difference between two neighboring electrocorticographic electrodes on primary visual cortex of an awake macaque monkey during one visual exploration of the photograph of two oranges (adapted and modified from (Brunet et al., 2013)). Green vertical line indicates stimulus onset, red vertical lines indicate saccades. Insets show the stimulus and superimposed the eye position trace around that time point in blue, and the eye position trace during this exploration so far in gray. Prior to stimulus appearance and free viewing, the monkey fixated on a small central dot.

Figure 2. Communication Through Coherence (CTC)

(A) Two presynaptic neuronal groups in a lower visual area provide input to a postsynaptic neuronal group in a higher visual area. The lower groups represent two visual stimuli, an apple and a pear. In each neuronal group, network excitation (red) triggers network inhibition (blue), which inhibits the local network. When inhibition decays, excitation restarts the gamma cycle. The gamma rhythm of the apple-representing presynaptic group has entrained the gamma rhythm in the postsynaptic group. Thereby, the apple-representing presynaptic group can optimally transmit its representation, whereas the pear-representing presynaptic group cannot transmit its representation. (B) A simplified illustration, in which network excitation and inhibition are combined into network excitability. Red vertical lines indicate excitatory neuron spiking, blue vertical lines inhibitory neuron spiking.

Figure 3. Inter-laminar delays might compensate for inter-areal feedforward and feedback delays

(A) Analysis of current source density (CSD) derived from laminar recordings in awake monkey area V1 (adapted and modified from (van Kerkoerle et al., 2014)). Laminar CSD was averaged relative to troughs in the gamma-filtered LFP from layer 4. The analysis reveals inter-laminar gamma-band synchronization with systematic delays as a function of distance from layer 4. (B) The inter-laminar delays might delay the supra- and infra-granular gamma phase such that reentrant feedback arrives at the excitable phase of the same, delayed, gamma cycle (Bastos et al., 2015b). Cortical depth is indicated by approximate position of the different cortical layers, abbreviated as L1 through L6. Arrows indicate the proposed flow of gamma-mediated signaling. Inter-areal arrows conform to the known laminar pattern of feedforward and feedback connections (Markov et al., 2014). Note that the CSD analyses do not reflect the finding that gamma-band spike-LFP coherence is stronger in superficial as compared to deep layers (Buffalo et al., 2011).

Figure 4. The gamma cycle implements pulsatile neuronal representations

(A-C) Awake monkey V1 single unit during visual stimulation with a drifting grating (adapted and modified from (Womelsdorf et al., 2012)). (A) Spike probability as function of the gamma phase in LFPs, which were recorded simultaneously from separate nearby electrodes. (B) The colored bar shows the partitioning of the gamma cycle into eight phase bins containing equal numbers of spikes (aligned to the phase in the gamma cycle to which spikes synchronized on average). Orientation tuning curves calculated separately for the eight gamma phase bins show a strong modulation of orientation selectivity with gamma phase, even though spike count was equal. (C) Orientation selectivity index (OSI) as function of the gamma phase bin, in which the spikes occurred.

Figure 5. Selective attention through selective inter-areal Granger-causal influences in the gamma band

Triplet recording of two sites in V1 (B, F) and one site in V4 (D, H), allowing the analysis of Granger-causal (GC) inter-areal influences (C, G) (adapted and modified from (Bosman et al., 2012)). (A-D) Two conditions with a single visual stimulus each, showing the stimulus selectivity of the recorded neuronal signals. (A) Illustration of the two conditions. The stimuli were behaviorally relevant and therefore attended, as indicated by their halo. Red and blue frames are not shown to the monkey, but used to label the corresponding spectra in the following panels. (B) Spectral power changes, relative to pre-stimulus baseline, for the two V1 sites. Each site showed visually induced gamma-band activity exclusively for one of the two stimuli. (C) GC influence spectra, showing the feedforward influences of V1 onto V4. (D) Spectral power change, relative to pre-stimulus baseline, for the V4 site. The site showed visually induced gamma-band activity that was very similar for the two stimuli. (E-H) Same as (A-D), but for two conditions with two visual stimuli and selective attention to one of them. (F) In V1, selective attention enhances gamma peak frequency (see also Figure 6A, B). (G) V1 exerts feedforward influence onto V4 almost exclusively through the gamma rhythm induced by the attended stimulus. (H) V4 responds equally strongly to both conditions. Previous studies have demonstrated that spike rates of single neurons in V4 predominantly represent the attended stimulus (Moran and Desimone, 1985; Reynolds et al., 1999), as indicated by the stimulus symbols above the panel.

Figure 6. The gamma-band peak frequency increases with attention and salience

(A, B) Awake macaque V1 LFP power changes (scaled to peak at a value of one) induced by a grating stimulus, when it was non-attended (blue) or attended (red) (adapted and modified from (Bosman et al., 2012)). (B) shows a detail of (A) at higher resolution. (C) Human MEG power change over early visual cortex as a function of time after stimulus onset. Note that the gamma peak frequency is higher at response onset than during the sustained response (adapted and modified from (van Pelt et al., 2012)). (D, E, F) Anesthetized macaque V1 LFP power, during visual stimulation with a grating of varying contrast (D), varying amount of superimposed noise (E), and varying size (F), as indicated by inset color legends (adapted and modified from (Jia et al., 2013b)). (G) Human MEG power change, estimated to emerge from primary visual cortex, during visual stimulation with a grating that is stationary (blue) or moving (red) (adapted and modified from (Swettenham et al., 2009)). (H) Awake macaque V1 LFP power during stimulation with a large grating that activated a recording site with a peripheral RF (blue) and another recording site with a foveal RF (red) (adapted and modified from (Lima et al., 2010)). (I) Anesthetized macaque V1 LFP gamma peak frequency (red line and left y-axis) as well as gamma power (blue line and right y-axis) as a function of stimulus orientation relative to the recording site's preferred orientation (adapted and modified from (Jia et al., 2013b)).

Figure 7. Theta-rhythmic phase reset turns gamma-frequency differences into latency differences

In the lower area, after a reset, the gamma rhythms representing different stimuli start at the same phase. The gamma rhythm representing the attended stimulus (green) is faster than the gamma rhythm representing the unattended stimulus (orange). This frequency difference translates into a latency difference. The input from the attended representation reaches the higher area first, transmits its representation and triggers inhibition to shut out the competing unattended representation.

Figure 8. Feedforward predominates in theta and gamma bands, feedback in the alpha-beta band

(A) Granger-causal influences between awake macaque areas V1 and DP. The influence in the V1-to-DP direction is through an anatomical feedforward-type projection and predominates in the theta and gamma bands, indicated by purple and orange backgrounds, respectively. The influence in the DP-to-V1 direction if through an anatomical feedback-type projection and predominates in the beta band, indicated by green background. (B) The Spearman-rank correlation, across area pairs, between an anatomical metric of the feedforward/feedback-character of an inter-areal projection (SLN) and an electrophysiological metric of the asymmetry in Granger-causal influences (DAI). A positive (negative) correlation value indicates that Granger-causal influences in the respective frequency are stronger in the anatomically-defined feedforward (feedback) direction. (A, B) are adapted and modified from (Bastos et al., 2015a). (C) Spike-LFP coherence from awake macaque area V2, for recordings from deep (blue) and superficial (red) layers. Spike-LFP coherence shows an alpha-beta band peak for deep layers and both a theta and a gamma peak for superficial layers (adapted and modified from (Buffalo et al., 2011)). (D) Awake macaque V4 LFP power during visual stimulation with a background stimulus (black) and additional electrical stimulation in V1 (five pulses at 200 Hz), which leads to power enhancement in the gamma band (red). (E) Awake macaque V1 LFP power during visual stimulation with a background stimulus (black) and additional electrical stimulation in V4 (five pulses at 200 Hz), which leads to power enhancement in the alpha-beta band (blue). (D, E) are adapted and modified from (van Kerkoerle et al., 2014).

Figure 9. A theta rhythm is visible in visual gamma, saccades and attentional sampling

(A) V1-V4 coherence as a function of frequency and of time in the 4 Hz theta cycle (adapted and modified from (Bosman et al., 2012)). (B) Histograms of inter-saccadic intervals (ISIs) for microsaccades and regular saccades during free viewing of natural scenes. (C) The histograms of (B) have been fitted with ex-Gaussian functions. The resulting parameter estimates are shown for microsaccades and saccades observed during several viewing conditions as indicated. Irrespective of condition, the Gaussian component's mean was around 145 ms, corresponding to 7 Hz. (B, C) are adapted and modified from (Otero-Millan et al., 2008). (D) Detection accuracy for equally probable contrast decrements on two bilateral stimuli, after an irrelevant flash at time zero. (E) Spectral analysis of the time-resolved detection accuracy from (D). The amplitude spectra reveal peaks close to 4 (D, E) are adapted and modified from (Landau and Fries, 2012).