Peak frequency in the theta and alpha bands correlates with human working memory capacity

Abstract

Theta oscillations in the local field potential of neural ensembles are considered key mediators of human working memory. Theoretical accounts arising from animal hippocampal recordings propose that the phase of theta oscillations serves to instantiate sequential neuronal firing to form discrete representations of items held online. Human evidence of phase relationships in visual working memory has enhanced this theory, implicating long theta cycles in supporting greater memory capacity. Here we use human magnetoencephalographic recordings to examine a novel, alternative principle of theta functionality. The principle we hypothesize is derived from information theory and predicts that rather than long (low frequency) theta cycles, short (high frequency) theta cycles are best suited to support high information capacity. From oscillatory activity recorded during the maintenance period of a visual working memory task we show that a network of brain regions displays an increase in peak 4-12 Hz frequency with increasing memory load. Source localization techniques reveal that this network comprises bilateral prefrontal and right parietal cortices. Further, the peak of oscillation along this theta-alpha frequency axis is significantly higher in high capacity individuals compared to low capacity individuals. Importantly while we observe the adherence of cortical neuronal oscillations to our novel principle of theta functioning, we also observe the traditional inverse effect of low frequency theta maintaining high loads, where critically this was located in medial temporal regions suggesting parallel, dissociable hippocampal-centric, and prefrontal-centric theta mechanisms.

Keywords: MEG; alpha; capacity; oscillations; theta; visual working memory.

Figure 1

Experimental design. (A) Experimental design. (B) Load-specific K, averaged across subjects. Error bars, here and in subsequent figures, depict SEM. (C) MEG sensor data: frequency spectra for maintenance period at each sensor, averaged over trial type and subjects; average is illustrated with the red line.

Figure 2

Sensor data. (A) SPM (threshold p < 0.005) in two dimensional channel space (up is anterior, left is left) showing a significant K × Band interaction over frontal and parietal sites. Arrow points to global maximum in right frontal site (z = 4.00; p = 0.000). (B) The power spectrum from the right frontal sensor overlaying the global maximum in (A) is plotted from 2 to 14 Hz for Left, low WM capacity and Right, high capacity individuals (high and low capacity defined by median split). Whereas low capacity individuals express 4–12 Hz peaks at (mean, SEM) 10.11 Hz (0.96), high capacity individuals achieve peaks at 12.44 Hz (0.40). Bandwidth measures from 4 to 12 Hz onset, defined as a rise in power greater than 50% of baseline (2–4 Hz) activity (i.e., the 3 dB point), to the peaks are illustrated for each group. Low capacity subjects have a narrowband occupancy (1.11 Hz) while high capacity subjects use a comparatively wideband signal (2.14 Hz).

Figure 3

Contralateral and ipsilateral sensor analysis. (A) SPM (threshold p < 0.01, one-sample t-test) showing K × Band interaction for stimulus arrays attended to in the right hemifield with significant effects observed bilaterally over frontal and occipito-parietal sensors and a maximum over left frontal cortex. (B) SPM (threshold p < 0.01, one-sample t-test) showing interaction for stimulus arrays attended to in the left hemifield with again significant effects observed bilaterally over frontal and occipito-parietal sensors but here the maximum is over contralateral right frontal cortex. (C,D) Significant differences (threshold p < 0.01, paired t-test) between the K × Band interaction are observed with peaks over contralateral sensors. (E) Average normalized spectra for loads of 2 (black line) and 6 (red line) demonstrating this effect at 1 Hz resolution for the theta–alpha frequencies included above (4–12 Hz). Spectra are averaged over frontal sensors from ipsilateral and contralateral sites for both attend right and attend left hemifield trials. Greater power at lower frequencies are observed for low (2) load trials while for high (6) load trials, power increases at higher theta/alpha frequencies. Individual subject spectra are included in Figure S1 in Supplementary material.

Figure 4

Neuroanatomical network showing increased 4–12 Hz power with increasing item retention. The SPM has been rendered onto a canonical T1 structural image (height threshold p < 0.015 uncorrected; extent threshold 15 contiguous voxels) and demonstrates activation bilaterally in occipital areas (x, y, z co-ordinates 2, −62, 14; z = 3.19; p = 0.001), extending into inferior temporal cortex (−58, −68, −4; z = 2.63; p = 0.004).

Figure 5

Neuroanatomical network subtending higher frequency responses for increasing item retention. (A) The SPM has been rendered onto a canonical T1 structural image (height threshold p < 0.015 uncorrected; extent threshold 15 contiguous voxels) and demonstrates a significant K × Band interaction in a prefrontal-parietal network in which low theta frequencies support low item retention and higher alpha frequencies support high item retention. Significant effects are observed in right (56, 28, 30; z = 2.92; p = 0.002) and left (−32, 22, 16; z = 2.78; p = 0.003) dorsolateral prefrontal cortex (dlPFC), and right inferior parietal cortex (60, −42, 44; z = 2.37; p = 0.009). (B) Power estimates from the peak voxel (right dlPFC) for each of the four sub-bands are plotted for the load at which subjects reached K_max minus that for load 2, showing dominant low frequencies at low retention levels and increasingly higher frequencies employed for high retention at K_max. (C) Power estimates from the peak voxel (right dlPFC) for frequency-specific theta power, for the six individuals with K_max at loads less than 6, for the next higher load than the load at which they achieve K_max (K_max+1) minus that at the load corresponding to K_max. Three subjects achieved K_max at load 4, and three subjects at load 3. These individuals failed to recruit higher alpha frequencies for higher loads. (D) Subject-specific capacity (K_max) is plotted against the high frequency sub-band (R = 0.50). Power estimates are from the peak voxel (right dlPFC) for the 10–12 Hz frequency range at load 6 minus the average 10–12 Hz power across all loads.

Figure 6

Medial temporal lobe shows predominant low frequency theta for increasing item retention. The SPM (threshold p < 0.005; extent threshold 15 voxels) is overlaid on a sagittal (x = 17) and coronal (y = −34) T1-weighted, canonical section to illustrate hippocampal activation in the opposite interaction to Figure 5A. Occipital and medial temporal regions express low frequency theta frequencies for higher retention requirements, i.e., for the negative K × Band interaction. Peak voxel in left occipital cortex(−34, −86, −12; z = 3.72; p = 0.000) and cluster peak in right medial temporal lobe (12, −32, −4; z = 3.56; p = 0.000).

Figure S1

Individual subject normalized spectra for ipsilateral and contralateral sites for attend left and attend right trials.

Figure S2

Working memory maintenance increases alpha activity over occipto-parietal sensors ipsilateral to the attended hemifield.