Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2021 May 5;2(2):tgab034.
doi: 10.1093/texcom/tgab034. eCollection 2021.

Electrophysiological Correlates of Rodent Default-Mode Network Suppression Revealed by Large-Scale Local Field Potential Recordings

Leila Fakhraei  1 , Miranda Francoeur  1 , Pragathi P Balasubramani  2 , Tianzhi Tang  1 , Sidharth Hulyalkar  1 , Nathalie Buscher  1 , Jyoti Mishra  2 , Dhakshin S Ramanathan  1
Affiliations

Electrophysiological Correlates of Rodent Default-Mode Network Suppression Revealed by Large-Scale Local Field Potential Recordings

Leila Fakhraei et al. Cereb Cortex Commun. .

Abstract

The default-mode network (DMN) in humans consists of a set of brain regions that, as measured with functional magnetic resonance imaging (fMRI), show both intrinsic correlations with each other and suppression during externally oriented tasks. Resting-state fMRI studies have previously identified similar patterns of intrinsic correlations in overlapping brain regions in rodents (A29C/posterior cingulate cortex, parietal cortex, and medial temporal lobe structures). However, due to challenges with performing rodent behavior in an MRI machine, it is still unclear whether activity in rodent DMN regions are suppressed during externally oriented visual tasks. Using distributed local field potential measurements in rats, we have discovered that activity in DMN brain regions noted above show task-related suppression during an externally oriented visual task at alpha and low beta-frequencies. Interestingly, this suppression (particularly in posterior cingulate cortex) was linked with improved performance on the task. Using electroencephalography recordings from a similar task in humans, we identified a similar suppression of activity in posterior cingulate cortex at alpha/low beta-frequencies. Thus, we have identified a common electrophysiological marker of DMN suppression in both rodents and humans. This observation paves the way for future studies using rodents to probe circuit-level functioning of DMN function.

Significance: Here we show that alpha/beta frequency oscillations in rats show key features of DMN activity, including intrinsic correlations between DMN brain regions, task-related suppression, and interference with attention/decision-making. We found similar task-related suppression at alpha/low beta-frequencies of DMN activity in humans.

Keywords: DMN; alpha; local field potentials; posterior cingulate; task-related interference.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Target electrode locations and behavioral task. (A) 3D rendering of a rat brain with the relative location of all 32 electrodes marked. Target sites had some general involvement in the following domains of behavior: sensorimotor (motor cortex, dorsolateral striatum, and subthalamic nucleus), reward (orbitofrontal cortex, nucleus accumbens, and ventromedial striatum), cognitive (A32D/prelimbic cortex, A32V/infralimbic cortex, M2/premotor cortex, anterior insula, medio-dorsal thalamus, and dorsomedial striatum), visual (visual cortex), and default mode (hippocampus, dentate gyrus, dorsal subiculum, and amygdala). (B) Coronal rat brain sections (adapted from Paxinos & Watson, 7th Edition, 2013) with placement of the 8 cannulas marked. ML and AP (mm) coordinates are noted relative to bregma. Individual depths of all 4 wires in each cannula are visualized with a red dot at their target brain region (32 targets). (C) General structure of the go/wait task. Task was self-paced. Animals triggered visual stimuli by entering a noseport. Visual stimuli indicated the trial type to be either a “go” or “wait” trial. Animals would receive a reward if they responded within 2 s on a go trial or waited for 2 s prior to responding on a wait trial. (D) Response time distribution for different trial types (Go and Wait) from 1 animal.
Figure 2
Figure 2
Alpha and beta suppression in DMN brain regions during task. (A,B). We performed a time–frequency decomposition in dorsomedial prefrontal cortex (A32D) and posterior cingulate cortex (A29C) (mean across 60 sessions, from 11 animals, data FDR-corrected across all times, frequencies, and electrodes. Nonsignificant values (FDR-adjusted P-value > 0.05) were set to 0 for the purpose of visualization). (A) On both go and wait trials, A29C (posterior cingulate cortex) shows distinct epochs of task-related suppression relative to baseline across theta, alpha, and beta-frequencies. (B) Shaded error bar shows mean posterior cingulate cortex (A29C) activity for “wait” trials (0–4000 ms) and “go” trials (0–2000 ms) at different frequencies, with 8–20 Hz frequency band highlighted by red bars. (C) A32D shows increased activity in alpha and beta-frequencies, but desynchronization at lower frequencies. (D) Mean TF activity within 8–20 Hz band plotted over time, showing for both wait and go trials, two distinct “peaks” of suppression. (E) Five examples of both go and wait trials from A29C. Gray line show the raw time-series and blue lines show the 8-20 Hz filtered activity from the same trials.
Figure 3
Figure 3
Alpha-power suppression across brain regions. (A) Average data from each electrode within alpha/low beta-frequencies (8–20 Hz) were plotted relative to trial onset for each electrode (n = 60 sessions) plotted separately for “go” and “wait” trials. We applied a one-sided t-test at each time point for each electrode (against the null hypothesis of 0) followed by an FDR-correction across 32 electrodes/200 time-points, with nonsignificant points set to 0. (B) Bar plots are displayed only for brain regions showing significant activation or suppression in in the 8–20 Hz band (Bonferroni adjusted for 32 brain regions). Mean/SEM and P-values for each electrode is displayed in Supplementary Table 1. Each electrode number (1–32) is labeled and grouped into cognitive, motor, reward, visual, or DMN functional categories. On both “go” and “wait” trials we found a significant task-related suppression of activity primarily in putative DMN brain regions.
Figure 4
Figure 4
Alpha-frequency wPLI. (A) In each session we calculated the wPLI, averaged over the first second poststimulus separately for “go” and “wait” trials. We then calculated the average wPLI for each pair of electrodes across sessions (n = 60) within the 8–20 Hz frequency band over a time window of 0–1000 ms poststimulus, to generate a 32 × 32 matrix of “mean” wPLI values between regions. We applied a one-sided t-test to each pairwise value (against the null hypothesis of 0, with FDR-correction applied, FDR-adjusted P-value < 0.05). Nonsignificant pairwise relationships were set to 0 for easy visualization. We found strong evidence of inter-regional connectivity between default-mode brain regions for both trial types at alpha-frequencies. (B) We plotted the graph of connectivity matrices above (using wPLI threshold of 0.15) to illustrate the strong inter-regional relationships between DMN brain regions at alpha-frequencies for “go” and “wait” trials separately. (C) We calculated the mean wPLI for “go” and “wait trials” specifically between A29C and all other brain regions (d.f. = 59) to further illustrate the strong inter-regional wPLI from this seed to other DMN brain regions. Each electrode number (1–32) is labeled and grouped into cognitive, motor, reward, visual, or DMN functional categories. Full details of wPLI values are in Supplementary Table 2. (D) Connectivity (wPLI) values were calculated within DMN regions and from DMN to other brain regions (grouped according to panel above). wPLI was calculated in the time window noted above for the 8–20 Hz frequency band. We found that DMN regions were more strongly connected with each other compared to with regions from other networks within the 8–20 Hz band.
Figure 5
Figure 5
Relationship between alpha-power in DMN regions and behavior on the task. (A) The response time distribution (8451 wait trials, 5858 go trials) used for this analysis. In general, we assumed that faster response time on go trials and slower response time on wait trials were associated with better performance on this task. (B,C) We calculated the relationship between power and response time across all trials (from all animals) for all brain regions (FDR-corrected for all electrodes/frequencies/time-points). A30C and Posterior parietal cortex (PPCx) showed the strongest inverse relationship between alpha activity and behavior (nonsignificant time-points set to 0). Specifically, we found that increased power in A30C was associated with slower RT for go trials (positive relationship) and faster RT on wait trials (negative relationship), clear evidence that greater alpha-power in this brain region is linked with interference on the task. (D) Anterior insula shows the opposite relationship with behavior, with greater alpha-power associated with faster RTs on go trials (negative relationship) and greater theta/alpha-power showing slower RTs on wait trials (positive relationship). All imagesc plots were corrected using an FDR-correction (P < 0.05, across all time, frequency, and electrodes).
Figure 6
Figure 6
Evidence for DMN suppression of alpha-oscillations in humans. (A) Behavior for animals and humans on the task. (B) Evidence of alpha/low beta-desynchronization (i.e., suppression relative to baseline) is shown in electrode POz, the electrode nearest to posterior cingulate cortex in humans. Power within this [8–20 Hz] frequency band (baseline subtracted) shows suppression in activity during the trial, strongest between 400 and 600 ms (shaded error bar shows mean/SEM, n = 65 subjects) (C) Similar desynchronization can be observed on wait trials, though with two main peaks at 400 to 600 and 1800 to 2000 ms; note that in case of go-trials the correct-response would trigger a new trial by max 1500 ms, hence analyses > 1500 ms were not relevant to these stimuli. (D) Scalp topography (topo map) of go trials within the 8–20 Hz frequency band between 400 and 600 ms, and corresponding source localization demonstrates significant sources within this time-frequency band in DMN brain regions (particularly posterior cingulate cortex, precuneus, and right inferior parietal lobule). (E) Scalp topographies and corresponding source localizations for wait trials are shown for the dual peak suppression time windows (P < 0.05).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Andrews-Hanna JR, Reidler JS, Huang C, Buckner RL. 2010a. Evidence for the default network’s role in spontaneous cognition. J Neurophysiol. 104.1:322–335. - PMC - PubMed
    1. Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL. 2010b. Functional-anatomic fractionation of the brain’s default network. Neuron. 65:550–562. - PMC - PubMed
    1. Anticevic A, Cole MW, Murray JD, Corlett PR, Wang X-J, Krystal JH. 2012. The role of default network deactivation in cognition and disease. Trends Cogn Sci. 16:584–592. - PMC - PubMed
    1. Balasubramani PP, Ojeda A, Grennan G, Maric V, Le H, Alim F, Zafar-Khan M, Diaz-Delgado J, Silveira S, Ramanathan D, et al. 2021. Mapping cognitive brain functions at scale. Neuroimage. 231:117641. - PMC - PubMed
    1. Barthas F, Kwan AC. 2017. Secondary motor cortex: where ‘Sensory’ meets ‘Motor’ in the rodent frontal cortex. Trends Neurosci. 40:181–193. - PMC - PubMed

LinkOut - more resources