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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

Experimental setup.(A) Schematic diagram of the custom-designed μECoG array. Sixty-four electrodes of 250-μm diameter were distributed across three separate polyimide fingers and arranged in a hexagonal grid (1.5-mm inter-electrode spacing). Holes were cut into the polyimide foils in the space between electrodes to allow for the placement of linear silicon probes. (B) A photo from the surgical implantation of the μECoG array. The general area for SC penetrations is shown by a blue box. Black lines indicate the lateral sulcus (LAT) and the suprasylvian sulcus (SSY). (C) Schematic diagram illustrating the placement of dual-shank 32-channel silicon probes in the SC. Probes were placed such that neural data could be acquired from both superficial (blue) and deep (green) layers of the SC simultaneously. (D) Schematic illustration of the placement of linear silicon probes in the visual cortex. Single-shank 32-channel probes (100-μm inter-electrode spacing) were advanced into the cortex through small holes in the μECoG array. Probes were advanced until the most superficial contacts were just above the pial surface, such that we recorded, in a single penetration, from superficial and deep visual cortex simultaneously. SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; PAG, periaqueductal gray.
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Figure 1: Experimental setup.(A) Schematic diagram of the custom-designed μECoG array. Sixty-four electrodes of 250-μm diameter were distributed across three separate polyimide fingers and arranged in a hexagonal grid (1.5-mm inter-electrode spacing). Holes were cut into the polyimide foils in the space between electrodes to allow for the placement of linear silicon probes. (B) A photo from the surgical implantation of the μECoG array. The general area for SC penetrations is shown by a blue box. Black lines indicate the lateral sulcus (LAT) and the suprasylvian sulcus (SSY). (C) Schematic diagram illustrating the placement of dual-shank 32-channel silicon probes in the SC. Probes were placed such that neural data could be acquired from both superficial (blue) and deep (green) layers of the SC simultaneously. (D) Schematic illustration of the placement of linear silicon probes in the visual cortex. Single-shank 32-channel probes (100-μm inter-electrode spacing) were advanced into the cortex through small holes in the μECoG array. Probes were advanced until the most superficial contacts were just above the pial surface, such that we recorded, in a single penetration, from superficial and deep visual cortex simultaneously. SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; PAG, periaqueductal gray.

Mentions: The superior colliculus (SC) presents itself as an interesting model to study the ongoing dynamics of cortical-subcortical functional interaction because it receives dense inputs from a wide range of sensory and motor cortical areas (13). In addition, the SC is indirectly connected to the cortex via other subcortical structures such as the pulvinar and lateral geniculate nucleus (14–17). Here, we hypothesize that neural activity in the cortex and SC is intrinsically coupled and that functional interaction along bottom-up (SC-to-cortex) and top-down (cortex-to-SC) pathways is conveyed through distinct physiological frequency bands. To test this hypothesis, we recorded spiking activity and local field potentials (LFPs) from all layers of the SC and visual cortex while simultaneously sampling LFPs from the entire posterior cortex using a custom-designed microelectrode array (μECoG; Fig. 1). We identified cortico-tectal functional coupling modes spanning several physiological carrier frequencies. High-frequency amplitude envelope correlation was strongly related to the correlated spiking activity of SC and cortex neurons, and mirrored patterns of anatomical connectivity, whereas lower-frequency coupling appeared less related to structural connectivity. Cortico-tectal functional interaction in the high-frequency band was parcellated by the phase of slow cortical oscillations, reflecting the subcortical entrainment of ongoing activity to cortical “up” and “down” states. As the first demonstration of the large-scale correlation structure of ongoing cortico-tectal neural activity, these findings highlight that the functional architecture of large-scale networks in the brain can be resolved through the correlation analysis of ongoing neural dynamics.


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)

Experimental setup.(A) Schematic diagram of the custom-designed μECoG array. Sixty-four electrodes of 250-μm diameter were distributed across three separate polyimide fingers and arranged in a hexagonal grid (1.5-mm inter-electrode spacing). Holes were cut into the polyimide foils in the space between electrodes to allow for the placement of linear silicon probes. (B) A photo from the surgical implantation of the μECoG array. The general area for SC penetrations is shown by a blue box. Black lines indicate the lateral sulcus (LAT) and the suprasylvian sulcus (SSY). (C) Schematic diagram illustrating the placement of dual-shank 32-channel silicon probes in the SC. Probes were placed such that neural data could be acquired from both superficial (blue) and deep (green) layers of the SC simultaneously. (D) Schematic illustration of the placement of linear silicon probes in the visual cortex. Single-shank 32-channel probes (100-μm inter-electrode spacing) were advanced into the cortex through small holes in the μECoG array. Probes were advanced until the most superficial contacts were just above the pial surface, such that we recorded, in a single penetration, from superficial and deep visual cortex simultaneously. SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; PAG, periaqueductal gray.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643805&req=5

Figure 1: Experimental setup.(A) Schematic diagram of the custom-designed μECoG array. Sixty-four electrodes of 250-μm diameter were distributed across three separate polyimide fingers and arranged in a hexagonal grid (1.5-mm inter-electrode spacing). Holes were cut into the polyimide foils in the space between electrodes to allow for the placement of linear silicon probes. (B) A photo from the surgical implantation of the μECoG array. The general area for SC penetrations is shown by a blue box. Black lines indicate the lateral sulcus (LAT) and the suprasylvian sulcus (SSY). (C) Schematic diagram illustrating the placement of dual-shank 32-channel silicon probes in the SC. Probes were placed such that neural data could be acquired from both superficial (blue) and deep (green) layers of the SC simultaneously. (D) Schematic illustration of the placement of linear silicon probes in the visual cortex. Single-shank 32-channel probes (100-μm inter-electrode spacing) were advanced into the cortex through small holes in the μECoG array. Probes were advanced until the most superficial contacts were just above the pial surface, such that we recorded, in a single penetration, from superficial and deep visual cortex simultaneously. SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; PAG, periaqueductal gray.
Mentions: The superior colliculus (SC) presents itself as an interesting model to study the ongoing dynamics of cortical-subcortical functional interaction because it receives dense inputs from a wide range of sensory and motor cortical areas (13). In addition, the SC is indirectly connected to the cortex via other subcortical structures such as the pulvinar and lateral geniculate nucleus (14–17). Here, we hypothesize that neural activity in the cortex and SC is intrinsically coupled and that functional interaction along bottom-up (SC-to-cortex) and top-down (cortex-to-SC) pathways is conveyed through distinct physiological frequency bands. To test this hypothesis, we recorded spiking activity and local field potentials (LFPs) from all layers of the SC and visual cortex while simultaneously sampling LFPs from the entire posterior cortex using a custom-designed microelectrode array (μECoG; Fig. 1). We identified cortico-tectal functional coupling modes spanning several physiological carrier frequencies. High-frequency amplitude envelope correlation was strongly related to the correlated spiking activity of SC and cortex neurons, and mirrored patterns of anatomical connectivity, whereas lower-frequency coupling appeared less related to structural connectivity. Cortico-tectal functional interaction in the high-frequency band was parcellated by the phase of slow cortical oscillations, reflecting the subcortical entrainment of ongoing activity to cortical “up” and “down” states. As the first demonstration of the large-scale correlation structure of ongoing cortico-tectal neural activity, these findings highlight that the functional architecture of large-scale networks in the brain can be resolved through the correlation analysis of ongoing neural dynamics.

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