Intrinsic connections make up the densest connectivity in any cortical area and are the most direct link between two cortical zones. The inputs and outputs of primary motor cortex (M1) are well studied, but the intrinsic connectivity within M1 remains critically understudied and consequently poorly understood. To fully understand the brain’s motor system, we must identify the organization and function of intrinsic connectivity within M1. M1 has a somatotopic organization wherein a given M1 zone outputs to a given muscle or group of muscles via the corticospinal tract. Within this organization, intrinsic M1 connectivity may bind together muscle representations across joints or within joints. To identify the rules that govern the spatial organization of intrinsic M1 connectivity, I used a novel multi-pronged approach combining intrinsic signal optical imaging (ISOI) and intracortical microstimulation (ICMS) to localize and quantify the intrinsic connectivity of dozens of sites in the living brain of the squirrel monkey. I have found that long-range intrinsic connections preferentially link M1 zones with functionally similar motor outputs. This result suggests that long-range intrinsic connections within M1 primarily serve to bind together muscles representations within the same joint. This result grants insight into both the organization and function of intrinsic connectivity within primary motor cortex, which is an essential piece of information in understanding the brain’s motor system as a whole.