Activity Dynamics and Signal Representation in a Striatal Network Model with Distance-Dependent Connectivity

Sebastian Spreizer, Martin Angelhuber, Jyotika Bahuguna, Ad Aertsen, Arvind Kumar
2017 eNeuro  
Visual Abstract Significance Statement Recent findings suggest that striatal activity is organized in spatially compact neuron clusters. Here, we show that striatal projection neurons should have a nonmonotonically changing distance-dependent connectivity to obtain spatially localized activity patterns in striatum. Among the different states a striatal network can show, asynchronous-irregular and transition activity states closely resemble striatal activity in the healthy state. In contrast,
more » ... ong cortical inputs as observed in Parkinson's disease drive the network into a winner-take-all state, in which the striatum loses its stimulus sensitivity. Thus, our model makes specific predictions about the spatial network connectivity in the striatum and provides new insights about how the striatum might make a transition from a healthy state to a Parkinson's disease state. Theory/New Concepts July/August 2017, 4(4) e0348-16.2017 1-15 The striatum is the main input nucleus of the basal ganglia. Characterizing striatal activity dynamics is crucial to understanding mechanisms underlying action selection, initiation, and execution. Here, we studied the effects of spatial network connectivity on the spatiotemporal structure of striatal activity. We show that a striatal network with nonmonotonically changing distance-dependent connectivity (according to a gamma distribution) can exhibit a wide repertoire of spatiotemporal dynamics, ranging from spatially homogeneous, asynchronous-irregular (AI) activity to a state with stable, spatially localized activity bumps, as in "winner-take-all" (WTA) dynamics. Among these regimes, the unstable activity bumps [transition activity (TA)] regime closely resembles the experimentally observed spatiotemporal activity dynamics and neuronal assemblies in the striatum. In contrast, striatal networks with monotonically decreasing distance-dependent connectivity (in a Gaussian fashion) can exhibit only an AI state. Thus, given the observation of spatially compact neuronal clusters in the striatum, our model suggests that recurrent connectivity among striatal projection neurons should vary nonmonotonically. In brain disorders such as Parkinson's disease, increased cortical inputs and high striatal firing rates are associated with a reduction in stimulus sensitivity. Consistent with this, our model suggests that strong cortical inputs drive the striatum to a WTA state, leading to low stimulus sensitivity and high variability. In contrast, the AI and TA states show high stimulus sensitivity and reliability. Thus, based on these results, we propose that in a healthy state the striatum operates in a AI/TA state and that lack of dopamine pushes it into a WTA state.
doi:10.1523/eneuro.0348-16.2017 pmid:28840190 pmcid:PMC5566799 fatcat:tnuyzq253jfadbihv2757f6ufi