Neuropsychiatric disorders arise from circuit defects established during development. However, risk-genes involved in circuit organization have not been thoroughly investigated due to the large cost of making transgenic animals for each genetic manipulation. We aimed to create a high-throughput CRISPR toolkit to investigate the effects of risk-gene modulation in the developing brain. This toolkit includes CRISPR knockout to study protein function, CRISPR knockin for protein localization, and CRISPR activation (CRISPRa) for gene dosage studies. We used in utero electroporation to introduce CRISPR agents into the developing brain and analyzed neuronal migration and axonal targeting phenotypes with fluorescent microscopy. We developed a sparse CRISPR knockout method to investigate gene function in the developing brain, validating this method with known phenotypes like Pten increased cell soma size and Dab1 neuronal migration defects. We also identified a novel axonal phenotype with Dctn2 knockout were knockout axons produced large varicosities in the corpus callosum. Similar callosal phenotypes were seen in patients with loss-of-function mutations of DCTN2. We then compared several common tags with more efficient CRISPR knockin. We find that the single-epitope HA tag has similar fluorescence intensity and higher knockin efficiency compared to the tandem-derivative 3xHA and mScarlet-I with β-Actin and IgLON4 knockin. Finally, we show that the transcriptional activator VPR frequently used with CRISPRa affects neuronal migration in a gRNA-independent manner, affecting the ability to identify phenotypes with changes in specific gene dosage. We also show that CRISPRa affects neuronal migration during development and will need to be optimized further to be used to investigate gene dosage of risk-genes. This work has provided a significant advance in the development of a CRISPR toolkit for investigating risk-genes in the developing brain and has identified important variables that should be taken into consideration when designing these experiments.