Abstract
The interconnectivity between excitatory and inhibitory neural networks informs mechanisms by which rhythmic bursts of excitatory activity can be produced in the brain. One such mechanism, Pyramidal Interneuron Network Gamma (PING), relies primarily upon reciprocal connectivity between the excitatory and inhibitory networks, while also including intra-connectivity of inhibitory cells. The causal relationship between excitatory activity and the subsequent burst of inhibitory activity is of paramount importance to the mechanism and has been well studied. However, the role of the intra-connectivity of the inhibitory network, while important for PING, has not been studied in detail, as most analyses of PING simply assume that inhibitory intra-connectivity is strong enough to suppress subsequent firing following the initial inhibitory burst. In this paper we investigate the role that the strength of inhibitory intra-connectivity plays in determining the dynamics of PING-style networks. We show that networks with weak inhibitory intra-connectivity exhibit variations in burst dynamics of both the excitatory and inhibitory cells that are not obtained with strong inhibitory intra-connectivity. Networks with weak inhibitory intra-connectivity exhibit excitatory rhythmic bursts with weak excitatory-to-inhibitory synapses for which classical PING networks would show no rhythmic activity. Additionally, variations in dynamics of these networks as the excitatory-to-inhibitory synaptic weight increases illustrates the important role that consistent pattern formation in the inhibitory cells serves in maintaining organized and periodic excitatory bursts. Finally, motivated by these results and the known diversity of interneurons, we show that a PING-style network with two inhibitory subnetworks, one strongly intra-connected and one weakly intra-connected, exhibits organized and periodic excitatory activity over a larger parameter regime than networks with a homogeneous inhibitory population. Taken together, these results serve to better articulate the role of inhibitory intra-connectivity in generating PING-like rhythms, while also revealing how heterogeneity amongst inhibitory synapses might make such rhythms more robust to a variety of network parameters.
Highlights
Summarized, the Pyramidal Interneuron Network Gamma (PING) mechanism states that synchronous, rhythmic dynamics of both the excitatory and inhibitory cell populations can be generated if the inhibitory cells spike only in response to excitatory cell activity, if excitatory cell activity quickly induces a synchronous inhibitory population burst, and if the inhibitory burst suppresses all excitatory cells
Networks with stronger inhibitory synaptic weight synchronize only when average intrinsic cell firing frequency is high. These results motivate the current study in which we describe how changing the I-I connectivity strength in an E-I network is the impetus behind changing pattern formation in the inhibitory network, which in turn affects the dynamics of the excitatory network
Our work here has shown that the strength of intra-connectivity amongst inhibitory neurons in a E-I network plays a pivotal role in controlling rhythmic PING-like dynamics
Summary
The importance of inhibitory interneurons in driving and modulating rhythmic electrical activity is well established in a variety of brain regions, including the hippocampus (Traub et al, 1998; Kopell et al, 2000; Bartos et al, 2007; Aton et al, 2013) and the cortex (Desimone and Duncan, 1995; Luck et al, 1997; Reynolds et al, 1999; Fries, 2005; Bosman et al, 2012). Summarized, the PING mechanism states that synchronous, rhythmic dynamics of both the excitatory and inhibitory cell populations can be generated if the inhibitory cells spike only in response to excitatory cell activity, if excitatory cell activity quickly induces a synchronous inhibitory population burst, and if the inhibitory burst suppresses all excitatory cells These requirements ensure that bursts of inhibitory activity directly follow excitatory cell activity, and this inhibition suppresses the excitatory cells for a sufficient duration so that all excitatory cells are set to the same point in their firing cycle, so that upon the release of inhibition their action potentials occur in close temporal proximity, resulting in synchronous firing
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