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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

Large-scale topography of high-frequency cortico-tectal amplitude envelope correlation.(A) Left: Average cortical topography of LFP amplitude correlation between superficial SC and μECoG array. Note the strongest amplitude correlation over posterior visual cortex. Middle: Average cortical topography of deep SC to μECoG LFP amplitude correlation. Note the presence of strong amplitude correlation in visual and suprasylvian cortical areas. Amplitude correlation effects extend anterior-medially along the suprasylvian gyrus toward a separate cluster of strong correlation in suprasylvian cortex. Right: Plot of the density of tectally projecting neurons across the cortical surface. Data were adapted with permission from (13). (B) Population-averaged (±SEM) strength of superficial SC-μECoG (left) and deep SC-μECoG (middle) high-frequency amplitude envelope correlation for different cortical areas. A map of the areal parcellation used in this analysis is shown on the right. Note the presence of strong correlation in early visual cortical areas for superficial SC-μECoG channel pairs. In contrast, deep SC-μECoG amplitude correlation was more widespread, encompassing visual, suprasylvian, and posterior parietal areas. (C) Left: Incidence of significant SC-μECoG high-frequency amplitude correlation as a function of SC depth. Right: Population-averaged spike/noise ratio in response to visual flash stimulation (flash onset at 0 s). Note that significant amplitude correlation with cortex was most prominent in intermediate/deep SC layers.
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Figure 4: Large-scale topography of high-frequency cortico-tectal amplitude envelope correlation.(A) Left: Average cortical topography of LFP amplitude correlation between superficial SC and μECoG array. Note the strongest amplitude correlation over posterior visual cortex. Middle: Average cortical topography of deep SC to μECoG LFP amplitude correlation. Note the presence of strong amplitude correlation in visual and suprasylvian cortical areas. Amplitude correlation effects extend anterior-medially along the suprasylvian gyrus toward a separate cluster of strong correlation in suprasylvian cortex. Right: Plot of the density of tectally projecting neurons across the cortical surface. Data were adapted with permission from (13). (B) Population-averaged (±SEM) strength of superficial SC-μECoG (left) and deep SC-μECoG (middle) high-frequency amplitude envelope correlation for different cortical areas. A map of the areal parcellation used in this analysis is shown on the right. Note the presence of strong correlation in early visual cortical areas for superficial SC-μECoG channel pairs. In contrast, deep SC-μECoG amplitude correlation was more widespread, encompassing visual, suprasylvian, and posterior parietal areas. (C) Left: Incidence of significant SC-μECoG high-frequency amplitude correlation as a function of SC depth. Right: Population-averaged spike/noise ratio in response to visual flash stimulation (flash onset at 0 s). Note that significant amplitude correlation with cortex was most prominent in intermediate/deep SC layers.

Mentions: We next computed the correlation of high-frequency LFP amplitude envelopes between all possible combinations of SC-μECoG and SC-intracortical recording sites. Figure 4 displays the average cortical topography of high-frequency LFP amplitude correlations from superficial SC to μECoG (Fig. 4A, left) and deep SC to μECoG channel pairs (Fig. 4A, middle). Superficial SC recording sites were correlated with μECoG contacts distributed over the entire visual cortex, with strongest correlation in cortical area 18 (amplitude correlation = 0.021 ± 0.003 SEM), slightly weaker correlation in higher visual (SSY: suprasylvian area, 0.014 ± 0.003) and posterior parietal areas (PPc: 0.012 ± 0.002), and almost no correlation in auditory cortical areas (0.005 ± 0.002) (Fig. 4B, left). In contrast, deep SC layers displayed amplitude correlation effects with a wider range of cortical areas, with strongest correlation to visual area 21 (0.022 ± 0.004 SEM) and posterior parietal areas (PPc = 0.021 ± 0.003, PPr = 0.022 ± 0.003) (Fig. 4B, middle). The cortical topography of deep SC to μECoG high-frequency correlation extended from early visual areas, through higher visual and multisensory areas along the suprasylvian gyrus toward somatosensory cortex, and reflecting the data presented in Fig. 2C, was significantly correlated with the topography of cortico-tectal anatomical connectivity (Fig. 4A, right; P = 0.003).


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)

Large-scale topography of high-frequency cortico-tectal amplitude envelope correlation.(A) Left: Average cortical topography of LFP amplitude correlation between superficial SC and μECoG array. Note the strongest amplitude correlation over posterior visual cortex. Middle: Average cortical topography of deep SC to μECoG LFP amplitude correlation. Note the presence of strong amplitude correlation in visual and suprasylvian cortical areas. Amplitude correlation effects extend anterior-medially along the suprasylvian gyrus toward a separate cluster of strong correlation in suprasylvian cortex. Right: Plot of the density of tectally projecting neurons across the cortical surface. Data were adapted with permission from (13). (B) Population-averaged (±SEM) strength of superficial SC-μECoG (left) and deep SC-μECoG (middle) high-frequency amplitude envelope correlation for different cortical areas. A map of the areal parcellation used in this analysis is shown on the right. Note the presence of strong correlation in early visual cortical areas for superficial SC-μECoG channel pairs. In contrast, deep SC-μECoG amplitude correlation was more widespread, encompassing visual, suprasylvian, and posterior parietal areas. (C) Left: Incidence of significant SC-μECoG high-frequency amplitude correlation as a function of SC depth. Right: Population-averaged spike/noise ratio in response to visual flash stimulation (flash onset at 0 s). Note that significant amplitude correlation with cortex was most prominent in intermediate/deep SC layers.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 4: Large-scale topography of high-frequency cortico-tectal amplitude envelope correlation.(A) Left: Average cortical topography of LFP amplitude correlation between superficial SC and μECoG array. Note the strongest amplitude correlation over posterior visual cortex. Middle: Average cortical topography of deep SC to μECoG LFP amplitude correlation. Note the presence of strong amplitude correlation in visual and suprasylvian cortical areas. Amplitude correlation effects extend anterior-medially along the suprasylvian gyrus toward a separate cluster of strong correlation in suprasylvian cortex. Right: Plot of the density of tectally projecting neurons across the cortical surface. Data were adapted with permission from (13). (B) Population-averaged (±SEM) strength of superficial SC-μECoG (left) and deep SC-μECoG (middle) high-frequency amplitude envelope correlation for different cortical areas. A map of the areal parcellation used in this analysis is shown on the right. Note the presence of strong correlation in early visual cortical areas for superficial SC-μECoG channel pairs. In contrast, deep SC-μECoG amplitude correlation was more widespread, encompassing visual, suprasylvian, and posterior parietal areas. (C) Left: Incidence of significant SC-μECoG high-frequency amplitude correlation as a function of SC depth. Right: Population-averaged spike/noise ratio in response to visual flash stimulation (flash onset at 0 s). Note that significant amplitude correlation with cortex was most prominent in intermediate/deep SC layers.
Mentions: We next computed the correlation of high-frequency LFP amplitude envelopes between all possible combinations of SC-μECoG and SC-intracortical recording sites. Figure 4 displays the average cortical topography of high-frequency LFP amplitude correlations from superficial SC to μECoG (Fig. 4A, left) and deep SC to μECoG channel pairs (Fig. 4A, middle). Superficial SC recording sites were correlated with μECoG contacts distributed over the entire visual cortex, with strongest correlation in cortical area 18 (amplitude correlation = 0.021 ± 0.003 SEM), slightly weaker correlation in higher visual (SSY: suprasylvian area, 0.014 ± 0.003) and posterior parietal areas (PPc: 0.012 ± 0.002), and almost no correlation in auditory cortical areas (0.005 ± 0.002) (Fig. 4B, left). In contrast, deep SC layers displayed amplitude correlation effects with a wider range of cortical areas, with strongest correlation to visual area 21 (0.022 ± 0.004 SEM) and posterior parietal areas (PPc = 0.021 ± 0.003, PPr = 0.022 ± 0.003) (Fig. 4B, middle). The cortical topography of deep SC to μECoG high-frequency correlation extended from early visual areas, through higher visual and multisensory areas along the suprasylvian gyrus toward somatosensory cortex, and reflecting the data presented in Fig. 2C, was significantly correlated with the topography of cortico-tectal anatomical connectivity (Fig. 4A, right; P = 0.003).

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