Influence of learning and experience on neuronal numerosity selectivity
Final Report Abstract
Numerosity-selective neurons in selected regions of the primate posterior parietal and prefrontal association cortices encode the number of elements in a stimulus. While data existed about trained monkeys, little was known about the development of numerosity selectivity in the brain before this project started. We set out to adapt our behavioral protocols to address questions about the role of learning, experience and behavioral context for numerosity representations. Using multiple-electrode techniques, we simultaneously recorded neuronal activity in naïve and later also learning monkeys from the posterior parietal cortex (area VIP) and the prefrontal cortices (PFC), areas known to be important for numerical categories. We wanted to find out if and how numerosity selectivity may change with training status and behavioral relevance, and how neuronal networks in different association cortices may become modified by experience. First, we explored whether numerosity-selective neurons do exist in the brains of numerically-naïve monkeys, i.e. monkeys that had never been trained to discriminate numerosity. Surprisingly, a proportion of neurons spontaneously encoded numerosity that was behaviorally irrelevant and not discriminated by the animals. Numerosity-selective neurons were present both in area VIP of the parietal and the lateral PFC of the frontal lobe of the primate brain without numerical training. Our results therefore showed for the first time that visual numerosity is spontaneously represented as a perceptual category in a dedicated parieto-frontal network. After we had demonstrated the existence of numerosity-selective neurons without numerical training, we hypothesized that active discrimination of numerosity would change response properties of neurons. To address this, we simultaneously recorded from the same recording sites in the PFC and VIP while numerically-naïve monkeys discriminated the color of a set of dots, and after numerosity training responded to the numerosity of equivalent dot collections. A comparison of the neuronal data before and after numerosity-training showed that PFC became more responsive to numerosity during active numerosity discrimination. In contrast to the PFC, no training effects were observed for VIP neurons, even though VIP neurons were also responsive to numerosity. Our results indicate elevated PFC participation with executive control, whereas VIP encodes numerosity as a perceptual category regardless of behavioral relevance. As a significant extension of the originally proposed research plan, we also measured the visual receptive fields (RFs) of the neurons in VIP and PFC recorded during the numerosity task. This now allows us to compare numerosity-selectivity with visuo-spatial characteristics of the neurons. We found unexpected discrepancies in the position and spatial layout of RFs of adjacent neurons. This heterogeneity was even more pronounced in PFC than in VIP, which suggests increasing deterioration of topographic maps along the visual cortical hierarchy. We also found that the increased receptive field heterogeneity in PFC relative to upstream VIP corresponded with distinct connectivity patterns between the two fundamental cell classes. These findings suggest that local receptive field topography vanishes with hierarchical distance from visual cortical input and argue for increasingly modified functional microcircuits in non-canonical association cortices that contrast primary visual cortex (V1). Future analyses will show if RFs correlate with numerosity selectivity. Preliminary data suggest that the presence or absence of RFs is hardly predictive of task-related activity. To sum up, we managed to answer the main questions of the project: Numerosity-selective neurons exist in monkeys without prior training in the laboratory, and experience shapes and amplifies neuronal representations only in the PFC, the brain’s central executive.
Publications
- (2013) Neuronal correlates of a visual 'sense of number' in primate parietal and prefrontal cortices. Proceedings of the National Academy of Sciences of the USA 110: 11187–11192
Viswanathan P., Nieder A.
(See online at https://doi.org/10.1073/pnas.1308141110) - (2015) Differential impact of behavioral relevance on quantity coding in primate frontal and parietal neurons. Current Biology 25: 1259–1269
Viswanathan P., Nieder A.
(See online at https://doi.org/10.1016/j.cub.2015.03.025)
