Limits...
Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling.

Sweeney-Reed CM, Zaehle T, Voges J, Schmitt FC, Buentjen L, Kopitzki K, Hinrichs H, Heinze HJ, Rugg MD, Knight RT, Richardson-Klavehn A - Elife (2015)

Bottom Line: Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN.Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC.These findings support an active processing role for the ATN during memory formation.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Otto von Guericke University, Magdeburg, Germany.

ABSTRACT
Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (Sweeney-Reed et al., 2014). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

No MeSH data available.


Event-related potentials (ERPs).(A) Frontal cortex. (B) Left ATN. (C) Left dorsomedial thalamic nucleus. (D) Right dorsomedial thalamic nucleus. blue = during successful encoding. red = during unsuccessful encoding.DOI:http://dx.doi.org/10.7554/eLife.07578.007
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4459033&req=5

fig3s1: Event-related potentials (ERPs).(A) Frontal cortex. (B) Left ATN. (C) Left dorsomedial thalamic nucleus. (D) Right dorsomedial thalamic nucleus. blue = during successful encoding. red = during unsuccessful encoding.DOI:http://dx.doi.org/10.7554/eLife.07578.007

Mentions: We calculated the correlation across participants between theta phase alignment at the time when it was greater during successful than during unsuccessful encoding (0.9–1.1 s) and CFC using Pearson's correlation coefficient. We focused on within-RATN theta-gamma coupling, which differed significantly between successful and unsuccessful encoding (Sweeney-Reed et al., 2014). Because we previously identified a theta/alpha (7–12 Hz) phase synchrony difference between successful and unsuccessful encoding early in the post-stimulus period, we also calculated the correlation between phase alignment of these oscillations and subsequent CFC. The CFC frequency ranges (means over 7–8 Hz and 40–50 Hz) were selected a priori in light of our previous results (Sweeney-Reed et al., 2014). During successful encoding, the correlation between early frontal theta/alpha phase alignment and CFC was significant (r = 0.84, p = 0.019; false discovery rate (FDR) corrected p-value = 0.02 with a maximum FDR level of q = 0.05, to account for the calculation of multiple correlations). No significant correlation was observed during unsuccessful encoding, nor was there a correlation with early RATN or late frontal theta phase alignment during either successful or unsuccessful encoding (Figure 2B–F). The correlation was significant, however, between late RATN theta phase alignment and CFC applying the same frequency cut-offs (r = 0.78, p = 0.039). With a maximum FDR level of q = 0.1, the FDR-adjusted p-value was 0.04. These correlations were then directly compared between successful and unsuccessful encoding by calculating a z-score using the Fisher z-transform for each correlation coefficient and comparing the difference, corrected for sample size, to the unit normal distribution; correlation was significantly greater during successful encoding (criterion p < 0.05). Finally, we identified a broadband (4–20 Hz) early poststimulus RATN phase alignment, but unlike later RATN theta phase alignment, neither it nor the event-related potentials (ERPs) differed significantly between successful and unsuccessful encoding (Figure 3, Figure 3—figure supplement 1). The ERP peak amplitude was correlated with the early RATN phase alignment during successful (r = 0.75, p < 0.0001) and during unsuccessful encoding (r = 0.70, p < 0.0001) (Figure 3). There was no significant correlation between frontal ERP amplitude and frontal phase alignment (p > 0.05).10.7554/eLife.07578.005Figure 2.Significance of correlation between theta (4–8 Hz) phase alignment and theta-gamma cross-frequency coupling (CFC) within the RATN.


Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling.

Sweeney-Reed CM, Zaehle T, Voges J, Schmitt FC, Buentjen L, Kopitzki K, Hinrichs H, Heinze HJ, Rugg MD, Knight RT, Richardson-Klavehn A - Elife (2015)

Event-related potentials (ERPs).(A) Frontal cortex. (B) Left ATN. (C) Left dorsomedial thalamic nucleus. (D) Right dorsomedial thalamic nucleus. blue = during successful encoding. red = during unsuccessful encoding.DOI:http://dx.doi.org/10.7554/eLife.07578.007
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4459033&req=5

fig3s1: Event-related potentials (ERPs).(A) Frontal cortex. (B) Left ATN. (C) Left dorsomedial thalamic nucleus. (D) Right dorsomedial thalamic nucleus. blue = during successful encoding. red = during unsuccessful encoding.DOI:http://dx.doi.org/10.7554/eLife.07578.007
Mentions: We calculated the correlation across participants between theta phase alignment at the time when it was greater during successful than during unsuccessful encoding (0.9–1.1 s) and CFC using Pearson's correlation coefficient. We focused on within-RATN theta-gamma coupling, which differed significantly between successful and unsuccessful encoding (Sweeney-Reed et al., 2014). Because we previously identified a theta/alpha (7–12 Hz) phase synchrony difference between successful and unsuccessful encoding early in the post-stimulus period, we also calculated the correlation between phase alignment of these oscillations and subsequent CFC. The CFC frequency ranges (means over 7–8 Hz and 40–50 Hz) were selected a priori in light of our previous results (Sweeney-Reed et al., 2014). During successful encoding, the correlation between early frontal theta/alpha phase alignment and CFC was significant (r = 0.84, p = 0.019; false discovery rate (FDR) corrected p-value = 0.02 with a maximum FDR level of q = 0.05, to account for the calculation of multiple correlations). No significant correlation was observed during unsuccessful encoding, nor was there a correlation with early RATN or late frontal theta phase alignment during either successful or unsuccessful encoding (Figure 2B–F). The correlation was significant, however, between late RATN theta phase alignment and CFC applying the same frequency cut-offs (r = 0.78, p = 0.039). With a maximum FDR level of q = 0.1, the FDR-adjusted p-value was 0.04. These correlations were then directly compared between successful and unsuccessful encoding by calculating a z-score using the Fisher z-transform for each correlation coefficient and comparing the difference, corrected for sample size, to the unit normal distribution; correlation was significantly greater during successful encoding (criterion p < 0.05). Finally, we identified a broadband (4–20 Hz) early poststimulus RATN phase alignment, but unlike later RATN theta phase alignment, neither it nor the event-related potentials (ERPs) differed significantly between successful and unsuccessful encoding (Figure 3, Figure 3—figure supplement 1). The ERP peak amplitude was correlated with the early RATN phase alignment during successful (r = 0.75, p < 0.0001) and during unsuccessful encoding (r = 0.70, p < 0.0001) (Figure 3). There was no significant correlation between frontal ERP amplitude and frontal phase alignment (p > 0.05).10.7554/eLife.07578.005Figure 2.Significance of correlation between theta (4–8 Hz) phase alignment and theta-gamma cross-frequency coupling (CFC) within the RATN.

Bottom Line: Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN.Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC.These findings support an active processing role for the ATN during memory formation.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Otto von Guericke University, Magdeburg, Germany.

ABSTRACT
Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (Sweeney-Reed et al., 2014). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

No MeSH data available.