The Generation and Modulation of Distinct Gamma Oscillations with Local, Horizontal, and Feedback Connections in the Primary Visual Cortex: A Model Study on Large-Scale Networks

Abstract

Gamma oscillation (GAMMA) in the local field potential (LFP) is a synchronized activity commonly found in many brain regions, and it has been thought as a functional signature of network connectivity in the brain, which plays important roles in information processing. Studies have shown that the response property of GAMMA is related to neural interaction through local recurrent connections (RC), feed-forward (FF), and feedback (FB) connections. However, the relationship between GAMMA and long-range horizontal connections (HC) in the brain remains unclear. Here, we aimed to understand this question in a large-scale network model for the primary visual cortex (V1). We created a computational model composed of multiple excitatory and inhibitory units with biologically plausible connectivity patterns for RC, FF, FB, and HC in V1; then, we quantitated GAMMA in network models at different strength levels of HC and other connection types. Surprisingly, we found that HC and FB, the two types of large-scale connections, play very different roles in generating and modulating GAMMA. While both FB and HC modulate a fast gamma oscillation (around 50-60 Hz) generated by FF and RC, HC generates a new GAMMA oscillating around 30 Hz, whose power and peak frequency can also be modulated by FB. Furthermore, response properties of the two GAMMAs in a network with both HC and FB are different in a way that is highly consistent with a recent experimental finding for distinct GAMMAs in macaque V1. The results suggest that distinct GAMMAs are signatures for neural connections in different spatial scales and they might be related to different functions for information integration. Our study, for the first time, pinpoints the underlying circuits for distinct GAMMAs in a mechanistic model for macaque V1, which might provide a new framework to study multiple gamma oscillations in other cortical regions.

Multiple gamma rhythms carry distinct spatial frequency information in primary visual cortex

“…This suggests that MG might be related to local E-I in the input layer [ 65 – 73 ], while LG might be related to horizontal connections in the output layer, which has long-distance connections on a larger spatial scale. The distinct mechanisms of LG and MG are consistent with the model prediction from a recent computational study [ 34 ]. The involvement of different neural circuits in V1 gamma rhythms also explains the finding that each gamma rhythm has a specific relationship to the spike activity ( S5 Fig ) and suggests that different gamma bands might be related to different neural functions.…”

“…Our study also showed that there are spike–LFP phase locking for the low and medium GCs in V1. According to previous studies on 2 gammas in V1 [ 33 , 34 ], the spatial scale of the communication for LG and MG might be different. LG generated in superficial layer of V1 might have a relative larger communication scale than that of MG.…”

“…There are 2 possible mechanisms for SF dependence in distinct gamma rhythms. The first is that there is generally a negative correlation between brain signals at different TF bands and their preferences for SFs, and the second is that the SF dependences of the 3 gamma rhythms reflect the characteristics of different neural circuits [ 34 , 59 , 66 ] that generate them. We verified that SF tuning of gamma rhythms is a property of the oscillatory components instead of the TF ( S11 and S12 Figs).…”

Thalamocortical and intracortical contributions to stimulus-evoked and oscillatory activity in rodent primary auditory cortex

“…An obvious candidate to explain our observations is the system of long-range horizontal cortical connections which are excitatory but terminate on inhibitory as well as excitatory neurons (Ajima and Tanaka, 2006;Kurt et al, 2008). In line with this idea, modeling work suggested differential roles of horizontal, feedback and feedforward connections for gamma oscillations depending on gamma frequency (Han et al, 2021). The activation of horizontally projecting layer II/III neurons has been shown to elicit repetitive inhibitory as well as excitatory postsynaptic potentials in the gamma frequency range (Adesnik and Scanziani, 2010).…”

“…We therefore speculate that both gamma responses play distinct roles during acoustic processing. It is noteworthy that two types of gamma oscillations with different tuning properties were also observed in the visual system (Jia et al, 2011;Han et al, 2021). Relatedly, in slices of the auditory cortex Ainsworth and colleagues (Ainsworth et al, 2011) could show that even individual columns contain two gamma rhythm generators with different oscillation frequencies.…”