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Intrinsic coupling modes reveal the functional architecture of cortico-tectal networks.

Stitt I, Galindo-Leon E, Pieper F, Engler G, Fiedler E, Stieglitz T, Engel AK - Sci Adv (2015)

Bottom Line: We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales.Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity.Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

ABSTRACT
In the absence of sensory stimulation or motor output, the brain exhibits complex spatiotemporal patterns of intrinsically generated neural activity. Analysis of ongoing brain dynamics has identified the prevailing modes of cortico-cortical interaction; however, little is known about how such patterns of intrinsically generated activity are correlated between cortical and subcortical brain areas. We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales. Ongoing cortico-tectal interaction was characterized by correlated fluctuations in the amplitude of delta, spindle, low gamma, and high-frequency oscillations (>100 Hz). Of these identified coupling modes, topographical patterns of high-frequency coupling were the most consistent with patterns of anatomical connectivity, reflecting synchronized spiking within cortico-tectal networks. Cortico-tectal coupling at high frequencies was temporally parcellated by the phase of slow cortical oscillations and was strongest for SC-cortex channel pairs that displayed overlapping visual spatial receptive fields. Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity. Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

No MeSH data available.


Related in: MedlinePlus

The dynamics of spontaneous SC neural activity are dominated by the phase of slow and spindle oscillations.(A) Population-averaged (±SEM) SC spike PLVs calculated using the phase of cortical (left) and local SC oscillations (right). The dashed line in each plot illustrates the level of significance (P < 0.01). For SC-μECoG channel pairs, significantly correlated and uncorrelated channel pairs are plotted separately. The black bar at the bottom of the SC-μECoG plot indicates the area in which correlated and uncorrelated curves are significantly different (P < 0.01). Note that spiking in amplitude-correlated channel pairs is more strongly locked to the phase of slow cortical oscillations. In addition, SC spiking activity is locked to the phase of local oscillations at the spindle frequency (~10 Hz). (B) Population-averaged cross-frequency phase-amplitude spectrograms calculated using the phase of μECoG oscillations and the amplitude of SC signals. Significantly correlated SC-μECoG channel pairs are shown on the left, uncorrelated channel pairs in the middle, and the difference between correlated and uncorrelated on the right. Note that SC-μECoG channel pairs that display strong high-frequency amplitude correlation also show significantly stronger coupling of SC oscillations above 8 Hz to the phase of slow cortical oscillations.
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Figure 7: The dynamics of spontaneous SC neural activity are dominated by the phase of slow and spindle oscillations.(A) Population-averaged (±SEM) SC spike PLVs calculated using the phase of cortical (left) and local SC oscillations (right). The dashed line in each plot illustrates the level of significance (P < 0.01). For SC-μECoG channel pairs, significantly correlated and uncorrelated channel pairs are plotted separately. The black bar at the bottom of the SC-μECoG plot indicates the area in which correlated and uncorrelated curves are significantly different (P < 0.01). Note that spiking in amplitude-correlated channel pairs is more strongly locked to the phase of slow cortical oscillations. In addition, SC spiking activity is locked to the phase of local oscillations at the spindle frequency (~10 Hz). (B) Population-averaged cross-frequency phase-amplitude spectrograms calculated using the phase of μECoG oscillations and the amplitude of SC signals. Significantly correlated SC-μECoG channel pairs are shown on the left, uncorrelated channel pairs in the middle, and the difference between correlated and uncorrelated on the right. Note that SC-μECoG channel pairs that display strong high-frequency amplitude correlation also show significantly stronger coupling of SC oscillations above 8 Hz to the phase of slow cortical oscillations.

Mentions: To further investigate the temporal dynamics of cortico-tectal functional connectivity, we computed the phase-locking value (PLV) of SC spiking activity to cortical oscillations. In general, SC spiking activity was strongly modulated by the phase of cortical oscillations at a frequency of about 0.8 Hz (Fig. 7A, left), matching the reported frequency of the slow cortical oscillation (21, 22). However, functionally coupled SC-μECoG channel pairs displayed significantly stronger phase locking to slow cortical oscillations than did uncorrelated channel pairs (correlated: PLV = 0.09 ± 0.002 SEM, uncorrelated: PLV = 0.05 ± 0.001, P < 0.01). Cortico-tectal slow oscillatory spike-phase locking was specific for endogenous cortical slow oscillations and displayed no temporal dependency to the frequency of artificial ventilation (fig. S6). In contrast to cortico-tectal spike-phase locking, SC spiking activity displayed significant phase locking to local oscillations at a frequency of about 10 Hz (PLV = 0.055 ± 0.002 SEM, P < 0.01) (Fig. 7A, right).


Intrinsic coupling modes reveal the functional architecture of cortico-tectal networks.

Stitt I, Galindo-Leon E, Pieper F, Engler G, Fiedler E, Stieglitz T, Engel AK - Sci Adv (2015)

The dynamics of spontaneous SC neural activity are dominated by the phase of slow and spindle oscillations.(A) Population-averaged (±SEM) SC spike PLVs calculated using the phase of cortical (left) and local SC oscillations (right). The dashed line in each plot illustrates the level of significance (P < 0.01). For SC-μECoG channel pairs, significantly correlated and uncorrelated channel pairs are plotted separately. The black bar at the bottom of the SC-μECoG plot indicates the area in which correlated and uncorrelated curves are significantly different (P < 0.01). Note that spiking in amplitude-correlated channel pairs is more strongly locked to the phase of slow cortical oscillations. In addition, SC spiking activity is locked to the phase of local oscillations at the spindle frequency (~10 Hz). (B) Population-averaged cross-frequency phase-amplitude spectrograms calculated using the phase of μECoG oscillations and the amplitude of SC signals. Significantly correlated SC-μECoG channel pairs are shown on the left, uncorrelated channel pairs in the middle, and the difference between correlated and uncorrelated on the right. Note that SC-μECoG channel pairs that display strong high-frequency amplitude correlation also show significantly stronger coupling of SC oscillations above 8 Hz to the phase of slow cortical oscillations.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 7: The dynamics of spontaneous SC neural activity are dominated by the phase of slow and spindle oscillations.(A) Population-averaged (±SEM) SC spike PLVs calculated using the phase of cortical (left) and local SC oscillations (right). The dashed line in each plot illustrates the level of significance (P < 0.01). For SC-μECoG channel pairs, significantly correlated and uncorrelated channel pairs are plotted separately. The black bar at the bottom of the SC-μECoG plot indicates the area in which correlated and uncorrelated curves are significantly different (P < 0.01). Note that spiking in amplitude-correlated channel pairs is more strongly locked to the phase of slow cortical oscillations. In addition, SC spiking activity is locked to the phase of local oscillations at the spindle frequency (~10 Hz). (B) Population-averaged cross-frequency phase-amplitude spectrograms calculated using the phase of μECoG oscillations and the amplitude of SC signals. Significantly correlated SC-μECoG channel pairs are shown on the left, uncorrelated channel pairs in the middle, and the difference between correlated and uncorrelated on the right. Note that SC-μECoG channel pairs that display strong high-frequency amplitude correlation also show significantly stronger coupling of SC oscillations above 8 Hz to the phase of slow cortical oscillations.
Mentions: To further investigate the temporal dynamics of cortico-tectal functional connectivity, we computed the phase-locking value (PLV) of SC spiking activity to cortical oscillations. In general, SC spiking activity was strongly modulated by the phase of cortical oscillations at a frequency of about 0.8 Hz (Fig. 7A, left), matching the reported frequency of the slow cortical oscillation (21, 22). However, functionally coupled SC-μECoG channel pairs displayed significantly stronger phase locking to slow cortical oscillations than did uncorrelated channel pairs (correlated: PLV = 0.09 ± 0.002 SEM, uncorrelated: PLV = 0.05 ± 0.001, P < 0.01). Cortico-tectal slow oscillatory spike-phase locking was specific for endogenous cortical slow oscillations and displayed no temporal dependency to the frequency of artificial ventilation (fig. S6). In contrast to cortico-tectal spike-phase locking, SC spiking activity displayed significant phase locking to local oscillations at a frequency of about 10 Hz (PLV = 0.055 ± 0.002 SEM, P < 0.01) (Fig. 7A, right).

Bottom Line: We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales.Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity.Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

ABSTRACT
In the absence of sensory stimulation or motor output, the brain exhibits complex spatiotemporal patterns of intrinsically generated neural activity. Analysis of ongoing brain dynamics has identified the prevailing modes of cortico-cortical interaction; however, little is known about how such patterns of intrinsically generated activity are correlated between cortical and subcortical brain areas. We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales. Ongoing cortico-tectal interaction was characterized by correlated fluctuations in the amplitude of delta, spindle, low gamma, and high-frequency oscillations (>100 Hz). Of these identified coupling modes, topographical patterns of high-frequency coupling were the most consistent with patterns of anatomical connectivity, reflecting synchronized spiking within cortico-tectal networks. Cortico-tectal coupling at high frequencies was temporally parcellated by the phase of slow cortical oscillations and was strongest for SC-cortex channel pairs that displayed overlapping visual spatial receptive fields. Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity. Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

No MeSH data available.


Related in: MedlinePlus