The speed of parietal theta frequency drives visuospatial working memory capacity

Nina Wolinski, Nicholas R Cooper, Paul Sauseng, Vincenzo Romei, Nina Wolinski, Nicholas R Cooper, Paul Sauseng, Vincenzo Romei

Abstract

The speed of theta brain oscillatory activity is thought to play a key role in determining working memory (WM) capacity. Individual differences in the length of a theta cycle (ranging between 4 and 7 Hz) might determine how many gamma cycles (>30 Hz) can be nested into a theta wave. Gamma cycles are thought to represent single memory items; therefore, this interplay could determine individual memory capacity. We directly tested this hypothesis by means of parietal transcranial alternating current stimulation (tACS) set at slower (4 Hz) and faster (7 Hz) theta frequencies during a visuospatial WM paradigm. Accordingly, we found that 4-Hz tACS enhanced WM capacity, while 7-Hz tACS reduced WM capacity. Notably, these effects were found only for items presented to the hemifield contralateral to the stimulation site. This provides causal evidence for a frequency-dependent and spatially specific organization of WM storage, supporting the theta-gamma phase coupling theory of WM capacity.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
(A) Theta–gamma phase coupling theory. The maximum number of items stored in WM is thought to be a function of the number of gamma cycles nested into a theta wave [1,2]. We tested this theory by applying slower (4 Hz) and faster (7 Hz) theta frequency tACS, aiming at modulating the speed of theta cycles (as per the entrainment hypothesis; see [10,12,13,19]) to allow higher/lower numbers of gamma cycles nested within a theta phase. Four-hertz tACS (yellow panel) should slow down theta oscillations, allowing more gamma cycles to nest within a theta cycle, relative to sham (green panel), enhancing WM capacity. Seven-hertz tACS (blue panel) should speed up theta oscillations, allowing fewer gamma cycles to nest within a theta cycle, relative to sham (green panel), worsening WM capacity. (B) Visual delayed match to sample task. Two arrays of coloured squares were situated on either side of a white fixation cross in the centre of a black screen. The number of squares in each array (memory load) was 4, 5, or 6, with 20 trials presented for each load. The task started with a fixation cross on the screen. Prior to presentation of the arrays, an arrow appeared on the screen (200 ms) to indicate which of the two upcoming arrays (left or right) needed to be memorised. The two arrays then appeared on the screen (100 ms), followed by a retention interval (900 ms), again followed by two arrays (left and right; 2,000 ms). Participants had to indicate whether the array in the cued hemifield had changed. (C) (Experimental Montage) and (D) (Control Montage): results (underlying data can be found at: https://osf.io/rm6qp/). K-values for each combination of load and hemisphere for each condition per participant were calculated with the formula: (hit rate − false alarms) * set size [20] (see Data analysis). Leftmost graphs depict mean and individual K-values obtained for trials presented on the left hemifield for each active stimulation condition after sham correction (Sham-corrected 4 Hz, Sham-corrected 7 Hz). Rightmost graphs depict mean and individual K-values obtained for trials presented on the right hemifield for each active stimulation condition after sham correction (Sham-corrected 4 Hz, Sham-corrected 7 Hz). Significant differences between conditions were observed for the Experimental Montage (C) but not for the Control Montage (D) and only for stimuli presented to the left hemifield (i.e., contralateral to the stimulated parietal site). For non-sham-corrected K and accuracy data, see S1A and S1B Fig (S1A and S1B Table), respectively (underlying data can be found at: https://osf.io/rm6qp/). *p < 0.05; ****p <0.0001. Error bars depict standard error of the mean. tACS, transcranial alternating current stimulation; WM, working memory.
Fig 2
Fig 2
(A) Electric field distribution calculation (NIC 2.0 Software: http://www.neuroelectrics.com/products/software/nic2/) for Experimental (left) and Control (right) electrode montages. The Experimental Montage (P4-supraorbital) shows (i) a more right-lateralised field distribution with (ii) maximum current over more posterior parietal areas relative to the control montage (P4-Cz). The Control Montage shows (i) some left-lateralised field distribution with (ii) maximum current over right superior parietal areas, thus more anterior to P4. These differences in electric field distribution might be responsible for the significantly different impact obtained across the two montages and may possibly explain the null effects obtained using the Control Montage. (B) Masked display with highlights of right IPS electric field distribution calculation (NIC 2.0 Software: http://www.neuroelectrics.com/products/software/nic2/), relative to the Experimental (left) and Control Montages (right). Here, it can be more closely appreciated how the Experimental Montage induced a maximum current over IPS, relative to the Control Montage. IPS, intraparietal sulcus; NIC, Neuroelectrics Instrument Controller; rIPS, right intraparietal sulcus.

References

    1. Lisman JE, Idiart MA. Storage of 7 +/- 2 short-term memories in oscillatory subcycles. Science. 1995; 267:1512–1515. .
    1. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A. 2010; 107: 3228–3233. doi: ;
    1. Sauseng P, Klimesch W, Heise KF, Gruber WR, Holz E, Karim AA, et al. Brain oscillatory substrates of visual short-term memory capacity. Curr Biol. 2009; 19: 1846–1852. doi: .
    1. Polanía R, Nitsche MA, Korman C, Batsikadze G, Paulus W. The importance of timing in segregated theta phase-coupling for cognitive performance. Curr Biol. 2012; 22: 1314–1318. doi: .
    1. Albouy P, Weiss A, Baillet S, Zatorre RJ. Selective Entrainment of Theta Oscillations in the Dorsal Stream Causally Enhances Auditory Working Memory Performance. Neuron. 2017. 94: 193–206.e5. doi: .
    1. Vosskuhl J, Huster RJ, Herrmann CS. Increase in short-term memory capacity induced by down-regulating individual theta frequency via transcranial alternating current stimulation. Front Hum Neurosci. 2015; 9: 257 doi: ;
    1. McCollough AW, Machizawa MG, Vogel EK. Electrophysiological measures of maintaining representations in visual working memory. Cortex. 2007; 43: 77–94. .
    1. Vogel EK, Machizawa MG. Neural activity predicts individual differences in visual working memory capacity. Nature. 2004; 428: 748–751. doi: .
    1. Vogel EK, McCollough AW, Machizawa MG. Neural measures reveal individual differences in controlling access to working memory. Nature. 2005; 438: 500–503. doi: .
    1. Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol. 2014; 24: 333–339. doi: .
    1. Minami S, Amano K. Illusory Jitter Perceived at the Frequency of Alpha Oscillations. Curr Biol. 2017; 27: 2344–2351.e4. doi: .
    1. Cecere R, Rees G, Romei V. Individual differences in alpha frequency drive crossmodal illusory perception. Curr Biol. 2015; 25: 231–235. doi: .
    1. Romei V, Thut G, Silvanto J. Information-Based Approaches of Noninvasive Transcranial Brain Stimulation. Trends Neurosci. 2016; 39:782–795. doi: .
    1. Todd JJ, Marois R. Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity. Cogn Affect Behav Neurosci. 2005; 5: 144–155. .
    1. DaSilva AF, Volz MS, Bikson M, Fregni F. Electrode positioning and montage in transcranial direct current stimulation. J Vis Exp. 2011; 51 doi: .
    1. Antal A, Paulus W. Transcranial alternating current stimulation (tACS). Front Hum Neurosci. 2013; 7: 317 doi: .
    1. Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol. 2016; 127: 1031–1048. doi: .
    1. Todd JJ, Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature. 2004; 428: 751–754. doi: .
    1. Thut G, Miniussi C. New insights into rhythmic brain activity from TMS-EEG studies. Trends Cogn Sci. 2009; 13:182–189. doi: .
    1. Cowan N. The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav Brain Sci. 2001; 24: 87–114; discussion 114–185. .
    1. Miranda PC, Mekonnen A, Salvador R, Ruffini G. The electric field in the cortex during transcranial current stimulation. Neuroimage. 2013; 70: 48–58. doi: .
    1. Ruhnau P, Neuling T, Fuscá M, Herrmann CS, Demarchi G, Weisz N. Eyes wide shut: Transcranial alternating current stimulation drives alpha rhythm in a state dependent manner. Sci Rep. 2016; 6: 27138 doi: .
    1. Kamiński J, Brzezicka A, Wróbel A. Short-term memory capacity (7 ± 2) predicted by theta to gamma cycle length ratio. Neurobiol Learn Mem. 2011; 95: 19 23. doi: .
    1. Brady TF, Konkle T, Alvarez GA. A review of visual memory capacity: Beyond individual items and towards structured representations. Journal of Vision. 2011; 11: 1–34.
    1. Samaha J, Postle BR. The Speed of Alpha-Band Oscillations Predicts the Temporal Resolution of Visual Perception. Curr Biol. 2015; 25: 2985–2990. doi: .
    1. Furman AJ, Meeker TJ, Rietschel JC, Yoo S, Muthulingam J, Prokhorenko M, et al. Cerebral peak alpha frequency predicts individual differences in pain sensitivity. Neuroimage. 2017; 167: 203–210. doi: .
    1. Lega BC, Jacobs J, Kahana M. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus. 2012; 22: 748–761. doi: .
    1. Ray S, Maunsell JH. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron. 2010; 67: 885–896. doi: .
    1. Jaušovec N, Jaušovec K. Increasing working memory capacity with theta transcranial alternating current stimulation (tACS). Biol Psychol. 2014; 96: 42–47. doi: .
    1. Jaušovec N, Jaušovec K, Pahor A. The influence of theta transcranial alternating current stimulation (tACS) on working memory storage and processing functions. Acta Psychol (Amst). 2014; 146: 1–6. doi: .
    1. Drew TW, McCollough AW, Vogel EK. Event-related potential measures of visual working memory. Clin EEG Neurosci. 2006; 37: 286–291. doi: .
    1. McCollough AW, Machizawa MG, Vogel EK. Electrophysiological measures of maintaining representations in visual working memory. Cortex. 2007; 43: 77–94. .
    1. Astle DE, Nobre AC, Scerif G. Subliminally presented and stored objects capture spatial attention. J Neurosci. 2010; 30: 3567–3571. doi: .
    1. Jost K, Bryck RL, Vogel EK, Mayr U. Are old adults just like low working memory young adults? Filtering efficiency and age differences in visual working memory. Cereb Cortex. 2011; 21: 1147–1154. doi: .
    1. Kar K, Krekelberg B. Transcranial electrical stimulation over visual cortex evokes phosphenes with a retinal origin. J Neurophysiol. 2012; 108: 2173–2178. doi: .
    1. Kanai R, Chaieb L, Antal A, Walsh V, Paulus W. Frequency-dependent electrical stimulation of the visual cortex. Curr Biol. 2008; 18: 1839–1843. doi: .
    1. Buschman TJ, Siegel M, Roy JE, Miller EK. Neural substrates of cognitive capacity limitations. Proc Natl Acad Sci U S A. 2011; 108: 11252–11255. doi: .
    1. Gaspar JM, Christie GJ, Prime DJ, Jolicœur P, McDonald JJ. Inability to suppress salient distractors predicts low visual working memory capacity. Proc Natl Acad Sci U S A. 2016; 113: 3693–3698. doi: .
    1. Luria R, Vogel EK. Visual search demands dictate reliance on working memory storage. J Neurosci. 2011; 31: 6199–6207. doi: .
    1. Lee EY, Cowan N, Vogel EK, Rolan T, Valle-Inclán F, Hackley SA. Visual working memory deficits in patients with Parkinson's disease are due to both reduced storage capacity and impaired ability to filter out irrelevant information. Brain. 2010; 133: 2677–2689. doi: .

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj