Long-range thalamocortical communication is central to anesthesia-induced loss of consciousness and its reversal. However, isolating the specific neural networks connecting thalamic nuclei with various cortical regions for state-specific anesthesia regulation is challenging, with the biological underpinnings still largely unknown. Here, simultaneous electroencephalogram-fuctional magnetic resonance imaging (EEG-fMRI) and deep brain stimulation are applied to the intralaminar thalamus in macaques under finely-tuned propofol anesthesia. This approach led to the identification of an intralaminar-driven network responsible for rapid arousal during slow-wave oscillations. A network-based RNA-sequencing analysis is conducted of region-, layer-, and cell-specific gene expression data from independent transcriptomic atlases and identifies 2489 genes preferentially expressed within this arousal network, notably enriched in potassium channels and excitatory, parvalbumin-expressing neurons, and oligodendrocytes. Comparison with human RNA-sequencing data highlights conserved molecular and cellular architectures that enable the matching of homologous genes, protein interactions, and cell types across primates, providing novel insight into network-focused transcriptional signatures of arousal.