Microcircuitry of agranular frontal cortex: contrasting laminar connectivity between occipital and frontal areas

Abstract

Neocortex is striking in its laminar architecture. Tracer studies have uncovered anatomical connectivity among laminae, but the functional connectivity between laminar compartments is still largely unknown. Such functional connectivity can be discerned through spontaneous neural correlations during rest. Previous work demonstrated a robust pattern of mesoscopic resting-state connectivity in macaque primary visual cortex (V1) through interlaminar cross-frequency coupling. Here we investigated whether this pattern generalizes to other cortical areas by comparing resting-state laminar connectivity between V1 and the supplementary eye field (SEF), a frontal area lacking a granular layer 4 (L4). Local field potentials (LFPs) were recorded with linear microelectrode arrays from all laminae of granular V1 and agranular SEF while monkeys rested in darkness. We found substantial differences in the relationship between the amplitude of gamma-band (>30 Hz) LFP and the phase of alpha-band (7-14 Hz) LFP between these areas. In V1, gamma amplitudes in L2/3 and L5 were coupled with alpha-band LFP phase in L5, as previously described. In contrast, in SEF phase-amplitude coupling was prominent within L3 and much weaker across layers. These results suggest that laminar interactions in agranular SEF are unlike those in granular V1. Thus the intrinsic functional connectivity of the cortical microcircuit does not seem to generalize across cortical areas.

Visuomotor Functions in the Frontal Lobe

“…Some researchers have applied the canonical cortical microcircuit derived from the primary visual cortex to frontal areas (e.g., Heinzle et al 2007), but there are clear differences in cortical architecture and organization between occipital and frontal areas (e.g., Elston 2003, Ninomiya et al 2015 apply to the motor cortex (Shipp 2005)? Further research will reveal whether the similarities or the differences are more important.…”

Neural Elements for Predictive Coding

“…As proposed previously, the fundamental ‘agranular’ architectural characteristic of motor cortex can be considered a developmental adaptation to the minimization of prediction error through action, with consequent recession of the input layer for the ascending pathway, granular layer 4 (Adams et al, 2013a; Shipp et al, 2013) and modification of intrinsic microcircuitry (Godlove et al, 2014; Beul and Hilgetag, 2015; Ninomiya et al, 2015). As gPC is proposed as a universal theory of cortical function the ideal should be to analyze the workings of a generic vertebrate (mammalian) sensory cortex (Shipp, 2007).…”

Developmental Changes in EEG Phase Amplitude Coupling and Phase Preference over the First Three Years After Birth

“…Moreover, underlying characteristics of PAC may reflect an area's functional configuration within neural networks. Phase preference, or the phase of the low frequency waveform corresponding to the largest amplitude of the high frequency waveform (Figure 1), has been found to differ by brain area (Ninomiya et al, 2015), coupling frequencies, and task performance (Lega et al, 2016). Additionally, phase preference can vary between cortical layers: recordings from multielectrode arrays implanted in the striate cortex V1 of macaque monkeys found layers IV and VI to exhibit opposing phase preferences with respect to alpha oscillations (Bollimunta et al, 2011).…”