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35 reviewsSUMMARYPooled optical screens have enabled the study of cellular interactions, morphology, or dynamics at massivescale, but they have not yet leveraged the power of highly plexed single-cell resolved transcriptomic readoutsto inform molecular pathways. Here, we present a combination of imaging spatial transcriptomics with paralleloptical detection of in situ amplified guide RNAs (Perturb-FISH). Perturb-FISH recovers intracellular effects thatare consistent with single-cell RNA-sequencing-based readouts of perturbation effects (Perturb-seq) in ascreen of lipopolysaccharide response in cultured monocytes, and it uncovers intercellular and density-dependent regulation of the innate immune response. Similarly, in three-dimensional xenograft models, Perturb-FISHidentifies tumor-immune interactions altered by genetic knockout. When paired with a functional readout in aseparate screen of autism spectrum disorder risk genes in human-induced pluripotent stem cell (hIPSC) astrocytes, Perturb-FISH shows common calcium activity phenotypes and their associated genetic interactions anddysregulated molecular pathways. Perturb-FISH is thus a general method for studying the genetic and molecular associations of spatial and functional biology at single-cell resolution.