The Effects of Population Tuning and Trial-by-Trial Variability on Information Encoding and Behavior

• DOI: 10.1523/jneurosci.0859-19.2019
• Publication Date: 2019-11-21T22:49:18Z
• Authors: Ramon Nogueira; Nicole E. Peltier; Akiyuki Anzai; Gregory C. DeAngelis; Julio Martínez-Tr...; Rubén Moreno-Bote
• Keywords: PFC; Male; Neurons; 0301 basic medicine; 570; 0303 health sciences; Behavior, Animal; Models, Neurological; Motion Perception; Discriminant Analysis; Prefrontal Cortex; Global activity; MT/V5; Macaca mulatta; Temporal Lobe; Macaca fascicularis; 03 medical and health sciences; Noise correlations; Visual Perception; Animals; Sensory processing; Attention; Female; Neural Networks, Computer; Psychomotor Performance

Identifying the features of population responses that are relevant to the amount of information encoded by neuronal populations is a crucial step toward understanding population coding. Statistical features, such as tuning properties, individual and shared response variability, and global activity modulations, could all affect the amount of information encoded and modulate behavioral performance. We show that two features in particular affect information: the modulation of population responses across conditions (population signal) and the inverse population covariability along the modulation axis (projected precision). We demonstrate that fluctuations of these two quantities are correlated with fluctuations of behavioral performance in various tasks and brain regions consistently across 4 monkeys (1 female and 1 maleMacaca mulatta; and 2 maleMacaca fascicularis). In contrast, fluctuations in mean correlations among neurons and global activity have negligible or inconsistent effects on the amount of information encoded and behavioral performance. We also show that differential correlations reduce the amount of information encoded in finite populations by reducing projected precision. Our results are consistent with predictions of a model that optimally decodes population responses to produce behavior.SIGNIFICANCE STATEMENTThe last two or three decades of research have seen hot debates about what features of population tuning and trial-by-trial variability influence the information carried by a population of neurons, with some camps arguing, for instance, that mean pairwise correlations or global fluctuations are important while other camps report opposite results. In this study, we identify the most important features of neural population responses that determine the amount of encoded information and behavioral performance by combining analytic calculations with a novel nonparametric method that allows us to isolate the effects of different statistical features. We tested our hypothesis on 4 macaques, three decision-making tasks, and two brain areas. The predictions of our theory were in agreement with the experimental data.