Cognition has a severely limited capacity: Adult humans can retain only about four items “in mind”. This limitation is fundamental to human brain function: Individual capacity is highly correlated with intelligence measures and capacity is reduced in neuropsychiatric diseases. Although human capacity limitations are well studied, their mechanisms have not been investigated at the single-neuron level. Simultaneous recordings from monkey parietal and frontal cortex revealed that visual capacity limitations occurred immediately upon stimulus encoding and in a bottom-up manner. Capacity limitations were found to reflect a dual model of working memory. The left and right halves of visual space had independent capacities and thus are discrete resources. However, within each hemifield, neural information about successfully remembered objects was reduced by adding further objects, indicating that resources are shared. Together, these results suggest visual capacity limitation is due to discrete, slot-like, resources, each containing limited pools of neural information that can be divided among objects.