Analog Numerical Representations in Rhesus Monkeys: Evidence for Parallel Processing

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Abstract
Monkeys have been introduced as model organisms to study neural correlates of numerical competence, but many of the behavioral characteristics of numerical judgments remain speculative. Thus, we analyzed the behavioral performance of two rhesus monkeys judging the numerosities 1 to 7 during a delayed match-to-sample task. The monkeys showed similar discrimination performance irrespective of the exact physical appearance of the stimuli, confirming that performance was based on numerical information. Performance declined smoothly with larger numerosities, and reached discrimination threshold at numerosity “4.” The nonverbal numerical representations in monkeys were based on analog magnitudes, object tracking process (“subitizing”) could not account for the findings because the continuum of small and large numbers shows a clear Weber fraction signature. The lack of additional scanning eye movements with increasing set sizes, together with indistinguishable neuronal response latencies for neurons with different preferred numerosities, argues for parallel encoding of numerical information. The slight but significant increase in reaction time with increasing numerosities can be explained by task difficulty and consequently time-consuming decision processes. The behavioral results are compared to single-cell recordings from the prefrontal cortex in the same subjects. Models for numerosity discrimination that may account for these results are discussed.