Single-cell coding of sensory, spatial and numerical magnitudes in primate prefrontal, premotor and cingulate motor cortices

Abstract

The representation of magnitude information enables humans and animal species alike to successfully interact with the external environment. However, how various types of magnitudes are processed by single neurons to guide goal-directed behavior remains elusive. Here, we recorded single-cell activity from the dorsolateral prefrontal (PFC), dorsal premotor (PMd) and cingulate motor (CMA) cortices in monkeys discriminating discrete numerical (numerosity), continuous spatial (line length) and basic sensory (spatial frequency) stimuli. We found that almost exclusively PFC neurons represented the different magnitude types during sample presentation and working memory periods. The frequency of magnitude-selective cells in PMd and CMA did not exceed chance level. The proportion of PFC neurons selectively tuned to each of the three magnitude types were comparable. Magnitude coding was mainly dissociated at the single-neuron level, with individual neurons representing only one of the three tested magnitude types. Neuronal magnitude discriminability, coding strength and temporal evolution were comparable between magnitude types encoded by PFC neuron populations. Our data highlight the importance of PFC neurons in representing various magnitude categories. Such magnitude representations are based on largely distributed coding by single neurons that are anatomically intermingled within the same cortical area.

Independent coding of absolute duration and distance magnitudes in the prefrontal cortex

“…Given that the domain specificity was consistent with that of Eiselt and Nieder (2016), the key aspect is likely to be whether the subject can simply match the stimulus to the other or compare their relative values within each magnitude-not the demands of flexible ruleswitching. To compare the relative magnitudes without interference , independent neural magnitudes are more efficient than a general network-a model consistent with childhood development of neural networks from holistic to fractionated, fine-tuned systems (Tsujimoto 2008;Tsujimoto et al 2007).…”

“…In contrast to other experimental designs, in which the studied property of a stimulus is not its duration but alternative ones, such as space or numbers (Dehaene et al 1998;Eiselt and Nieder 2016;Tudusciuc and Nieder 2009), the duration of the stimulus can only be determined after its presentation. Thus the working memory period is the only epoch in which the neural representation of duration and distance can be compared.…”

“…Two studies (Eiselt and Nieder 2016;Tudusciuc and Nieder 2009) assessed the representation of space and numbers. The Tudusciuc and Nieder (2009) study, using a match-to-sample task, reported that 20% of selective neurons that were recorded in the PF represented numbers and line length, pointing to a generalist function of the PF in the representation of magnitude.…”

“…The Tudusciuc and Nieder (2009) study, using a match-to-sample task, reported that 20% of selective neurons that were recorded in the PF represented numbers and line length, pointing to a generalist function of the PF in the representation of magnitude. Subsequently, Eiselt and Nieder (2016) evaluated the representation of numbers, line length, and spatial frequency, adopting a more demanding paradigm than the match-tosample task of Tudusciuc and Nieder (2009). In this new task (Eiselt and Nieder 2016), monkeys were required to report whether a test quantity was "greater than" or "less than" a sample quantity, depending on the rule that was cued.…”

“…Subsequently, Eiselt and Nieder (2016) evaluated the representation of numbers, line length, and spatial frequency, adopting a more demanding paradigm than the match-tosample task of Tudusciuc and Nieder (2009). In this new task (Eiselt and Nieder 2016), monkeys were required to report whether a test quantity was "greater than" or "less than" a sample quantity, depending on the rule that was cued. In contrast to their previous study, they found no overlap among populations of neurons that encoded each magnitude.…”