Goal-directed behavior requires integrating sensory information with prior knowledge about the environment. Behavioral biases that arise from these priors could increase positive outcomes when the priors match the true structure of the environment, but mismatches also happen frequently and could cause unfavorable outcomes. Biases that reduce gains and fail to vanish with training indicate fundamental suboptimalities arising from ingrained heuristics of the brain. Here, we report systematic, gain-reducing choice biases in highly-trained monkeys performing a motion direction discrimination task where only the current stimulus is behaviorally relevant. The monkey's bias fluctuated at two distinct time scales: slow, spanning tens to hundreds of trials, and fast, arising from choices and outcomes of the most recent trials. Our finding enabled single trial prediction of biases, which influenced the choice especially on trials with weak stimuli. The pre-stimulus activity of neuronal ensembles in the monkey prearcuate gyrus represented these biases as an offset along the decision axis in the state space. This 2 offset persisted throughout the stimulus viewing period, when sensory information was integrated, leading to a biased choice. The pre-stimulus representation of historydependent bias was functionally indistinguishable from the neural representation of upcoming choice before stimulus onset, validating our model of single-trial biases and suggesting that pre-stimulus representation of choice could be fully defined by biases inferred from behavioral history. Our results indicate that the prearcuate gyrus reflects intrinsic heuristics that compute bias signals, as well as the mechanisms that integrate them into the oculomotor decision-making process.Addressing these questions requires developing a task in which heuristic biases are not rewarding. Biases that increase reward rate encourage alteration of decision strategies based on task structure, complicating generalization of results across tasks.But systematic biases that persist with training and are non-rewarding (or even reduce gain) provide an opportunity to explore the heuristics that shape history-dependent biases. Addressing our questions also requires single trial quantification of the magnitude of bias, as well as recording from neural ensembles in brain regions that represent both the bias and the decision-making process. Single trial quantification of 3 the magnitude of bias necessitates development of behavioral models that can accurately predict the bias on individual trials. Although many studies attempted to do so (Gold et al., 2008a; Jasper et al., 2019; Lueckmann et al., 2018), there are few comprehensive models that achieve sufficient accuracy, often because they ignore one or more key factors that shape the bias. Additionally, past studies on the neural representation of bias focused largely on single neuron activity (Eskandar and Assad, 1999; Hanks et al., 2011; Lueckmann et al., 2018; Nogueira et al., 2017; Padoa-Schioppa, 2013; Shadlen and Ne...