During behavior, the oculomotor system is tasked with selecting objects from an ever-changing visual field and guiding eye movements to these locations. The attentional priority given to visual targets during selection can be strongly influenced by external stimulus properties or internal goals based on previous experience. Although these exogenous and endogenous drivers of selection are known to operate across partially overlapping time scales, the form of their interaction over time remains poorly understood. Using a novel choice task that simultaneously manipulates stimulus- and goal-driven attention, we demonstrate that exogenous and endogenous attentional biases change linearly as a function of time after stimulus onset and have an additive influence on the visual selection process in rhesus macaques (Macaca mulatta). We present a family of computational models that quantify this interaction over time and detail the history-dependence of both processes. The computational models reveal the existence of a critical 140-180 ms attentional “switching” time, when stimulus and goal-driven processes simultaneously favor competing visual targets. These results suggest that the brain uses a linear sum of attentional biases to guide visual selection.
Coherent neuronal dynamics play an important role in complex cognitive functions. Optogenetic stimulation promises to provide new ways to test the functional significance of coherent neural activity. However, the mechanisms by which optogenetic stimulation drives coherent dynamics remain unclear, especially in the nonhuman primate brain. Here, we perform computational modeling and experiments to study the mechanisms of optogenetic-stimulation-driven coherent neuronal dynamics in three male nonhuman primates. Neural responses arise from stimulation-evoked, temporally dynamic excitatory (E) and inhibitory (I) activity. Spiking activity is more likely to occur during E/I imbalances. Thus the relative difference in the driven E and I responses precisely controls spike timing by forming a brief time interval of increased spiking likelihood. Experimental results agree with parameter-dependent predictions from the computational models. These results demonstrate that optogenetic stimulation driven coherent neuronal dynamics are governed by the temporal properties of E/I activity. Transient imbalances in excitatory and inhibitory activity may provide a general mechanism for generating coherent neuronal dynamics without the need for an oscillatory generator.
30Coherent neuronal dynamics play an important role in complex cognitive functions, but the 31 causal role of neuronal coherence is unclear. Optogenetic stimulation allows causal tests of the 32 functional significance of coherent neuronal activity. While non-human primates are important 33 for studying the neural mechanisms of complex cognitive functions, optogenetic perturbation of 34 neuronal dynamics has had limited application in this animal model. Here, we develop a 35 computational framework and perform experiments to test how optogenetic stimulation perturbs 36 coherent neuronal dynamics. We show that stimulation-evoked neural responses arise from 37 temporal windows of excitatory and inhibitory activity that vary parametrically with optogenetic 38 stimulation parameters. We experimentally identify the effective temporal window of excitation 39 and inhibition and use the window in a computational model to design model-based stimulation 40 sequences. These results demonstrate optogenetic perturbations of coherent neuronal 41 dynamics and advance the use of optogenetic tools to study complex cognitive functions in the 42 primate brain. 43 44 7 132 Figure 1. Excitation and inhibition drive coherent neuronal dynamics. (A) During spontaneous 133 activity, synaptic inputs drive activity in a local network. We model spiking as being generated from 134 a Poisson process with a constant rate and LFP as being generated from a Brown noise process. 135 Under these assumptions, spontaneous spiking is not coherent with spontaneous LFP. (B) To 136 model optogenetic stimulation of a population of transduced neurons, we simulated pulsatile 137 responses generated by direct activation of ChR2 channels and synaptic activity. Pulsatile 138 responses are convolved with a stimulation sequence. The summed excitatory and inhibitory (E-I, 139 black) components comprise the simulated LFP. The individual E (blue) and I (red) activity govern 140 the variable spiking rate in the Poisson process which generates coherent spiking. (C) 141Spontaneous activity in the model has no spike-field coherence. (D) Optogenetic stimulation drives 142 correlated fields and spiking, leading to frequency selective spike-field coherence.
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