Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas

Abstract

Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral and dorsal stream visual areas are differentially affected by inter-areal influences in the alpha-beta band.

MEG-measured visually induced gamma-band oscillations in chronic schizophrenia: Evidence for impaired generation of rhythmic activity in ventral stream regions

“…This has led to the conclusion that gamma-band activity may essentially be involved in feedforward propagation of sensory activity along the visual hierarchy (Michalareas et al, 2016) which is consistent with the laminar expression profile (Markov et al, 2014). More specifically, high frequency oscillations occur predominantly in granular layers 3 and 4, while alpha (8-12 Hz)/beta (13-30 Hz) oscillations occur predominantly in infra-granular layers 5 and 6 (Bastos et al, 2015;van Kerkoerle et al, 2014).…”

Alterations in Functional Cortical Hierarchy in Hemiparkinsonian Rats

“…Interestingly, on the basis of structural connectivity data, a cortical circuit model has recently been proposed in which information flow is directed from somatomotor and sensory areas to association areas in prefrontal and temporal cortex, defining a hierarchical organization (Chaudhuri et al, 2015). Modeling based on structural connectivity among visual, parietal, and frontal areas has been shown to correlate very well with functional modeling (Markov et al, 2014;Bastos et al, 2015;Michalareas et al, 2016). Together, these findings suggest that directional connectivity and hierarchical functional organization might play an important role in changes affecting networks encompassing frontal association and motor regions that occur as a consequence of loss of dopamine.…”

“…2. For each area combination, we then computed the directional asymmetry index (DAI) as DAI m,k ϭ (GC-in m,k Ϫ GC-out m,k )/ (GC-in m,k ϩ GC-out m,k ), as in Bastos et al (2015) and Michalareas et al (2016). 3.…”

“…A value of 1 indicates that an area tends to be a receiver (i.e., sits at a top of the cortical hierarchy) (Bastos et al, 2015; Michalareas et al, 2016). These values are shown in Figure 7A, B.…”

“…Hemispheric asymmetries were examined at three levels: power, connectivity, and Granger causal (GC) influences. For determining the hierarchical position of an area in the network, the pattern of directed influences was established by using GC influence data to calculate the "directed asymmetry index," a measure that has been successfully used in correlating functional to structural hierarchical modeling among visual, parietal, and frontal areas (Markov et al, 2014;Bastos et al, 2015;Michalareas et al, 2016).…”