Abstract
Synchronous oscillations in neural populations are considered being controlled by inhibitory neurons. In the granular layer of the cerebellum, two major types of cells are excitatory granular cells (GCs) and inhibitory Golgi cells (GoCs). GC spatiotemporal dynamics, as the output of the granular layer, is highly regulated by GoCs. However, there are various types of inhibition implemented by GoCs. With inputs from mossy fibers, GCs and GoCs are reciprocally connected to exhibit different network motifs of synaptic connections. From the view of GCs, feedforward inhibition is expressed as the direct input from GoCs excited by mossy fibers, whereas feedback inhibition is from GoCs via GCs themselves. In addition, there are abundant gap junctions between GoCs showing another form of inhibition. It remains unclear how these diverse copies of inhibition regulate neural population oscillation changes. Leveraging a computational model of the granular layer network, we addressed this question to examine the emergence and modulation of network oscillation using different types of inhibition. We show that at the network level, feedback inhibition is crucial to generate neural oscillation. When short-term plasticity was equipped on GoC-GC synapses, oscillations were largely diminished. Robust oscillations can only appear with additional gap junctions. Moreover, there was a substantial level of cross-frequency coupling in oscillation dynamics. Such a coupling was adjusted and strengthened by GoCs through feedback inhibition. Taken together, our results suggest that the cooperation of distinct types of GoC inhibition plays an essential role in regulating synchronous oscillations of the GC population. With GCs as the sole output of the granular network, their oscillation dynamics could potentially enhance the computational capability of downstream neurons.
Highlights
The capacity of the brain to accommodate information precisely within a limited time window is important for reliable execution of complex sensory and motor behaviors [1, 2]
Together with current literature in research on the cerebellum, neural synchronous oscillation, and cross-frequency coupling, our results indicate that distinct types of inhibition could contribute to rich dynamics of the cerebellum and promote the cerebellum to play a functional character of cognition modulator in the communication with other brain areas
There is still a lack of understanding of how oscillation dynamics of granular cells (GCs) is regulated by a cohort of various types of inhibition together. We addressed this question with a network model of GCs and Golgi cells (GoCs) equipped with different scenarios of inhibition, feedback inhibition (FBI) and FFI between GCs and GoCs, and gap junctions between GoCs
Summary
The capacity of the brain to accommodate information precisely within a limited time window is important for reliable execution of complex sensory and motor behaviors [1, 2]. When the cerebellar cortex is injured, the movement loses precision and becomes uncoordinated and incorrectly timed, occurring in both humans [3,4,5] and animals [6, 7]. It indicates that the cerebellum has an extraordinary capability to accurately represent and process timing information during behaviors [8,9,10]. One typical precise timing activity in neuron population dynamics is synchronous oscillation, in which neural populations fire spikes as a pacemaker in time. Oscillations can be modulated by the balance of excitation and inhibition in cells [31,32,33,34]
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