Primate lateral intraparietal area (LIP) has been directly linked to perceptual categorization and decision-making. However, the intrinsic LIP circuitry that gives rise to the flexible generation of motor responses to sensory instruction remains unclear. Using retrograde tracers, we delineate two distinct operational compartments based on different intrinsic connectivity patterns of dorsal and ventral LIP. These connections form an anatomical loop with a sensory-like, point-to-point projection from ventral to dorsal LIP and an asymmetric, widespread projection in reverse. In neurophysiological recordings, LIP neurons exhibit motor response fields spatially distinct from their sensory receptive field. Different associations of motor response and receptive fields in single neurons tile visual space. Ventral LIP neurons tend to have motor response fields distant from their sensory receptive fields. This circuit provides the neural substrate to generate the dynamic processes for flexible allocation of attention and motor responses in response to salient or instructive visual input across the visual field.