Normalization by valence and motivational intensity in the sensorimotor cortices (PMd, M1, and S1)

Zhao Yao,Joseph Thachil Francis,John P Hessburg

doi:10.1038/s41598-021-03200-3

Zhao Yao, Joseph Thachil Francis + Show 1 more

Open Access

https://doi.org/10.1038/s41598-021-03200-3

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Abstract

Our brain’s ability to represent vast amounts of information, such as continuous ranges of reward spanning orders of magnitude, with limited dynamic range neurons, may be possible due to normalization. Recently our group and others have shown that the sensorimotor cortices are sensitive to reward value. Here we ask if psychological affect causes normalization of the sensorimotor cortices by modulating valence and motivational intensity. We had two non-human primates (NHP) subjects (one male bonnet macaque and one female rhesus macaque) make visually cued grip-force movements while simultaneously cueing the level of possible reward if successful, or timeout punishment, if unsuccessful. We recorded simultaneously from 96 electrodes in each the following: caudal somatosensory, rostral motor, and dorsal premotor cortices (cS1, rM1, PMd). We utilized several normalization models for valence and motivational intensity in all three regions. We found three types of divisive normalized relationships between neural activity and the representation of valence and motivation, linear, sigmodal, and hyperbolic. The hyperbolic relationships resemble receptive fields in psychological affect space, where a unit is susceptible to a small range of the valence/motivational space. We found that these cortical regions have both strong valence and motivational intensity representations.

Highlights

Neural networks within the primary sensorimotor cortices need to function within a limited dynamic range while encoding multiple forms of information such as kinematics and k inetics[1,2,3,4]
The periods used in our analysis presented here were not during any actual movement produced by the non-human primates (NHP)
Example single units from the three brain regions (PMd, M1, and S1) for the two NHPs are separated into units that had a qualitative motivational intensity relationship with cued reward and punishment (Fig. 2 NHP S S1 post-cue) or a valence relationship that is the neural rate either increased or decreased in a simple manner as trial valence increased, such as R0P3 with the lowest valence and R3P0 with the highest (Fig. 2 NHP P M1 pre-result)

Summary

Introduction

Neural networks within the primary sensorimotor cortices need to function within a limited dynamic range while encoding multiple forms of information such as kinematics and k inetics[1,2,3,4]. The nervous system could, in part, increase its information-carrying capacity by utilizing a temporal code, which would be less sensitive to a limited dynamic range than a rate c ode[5] Another possibility is provided by divisive n ormalization[6], where the input from another region and/or from the local population can dynamically normalize the network, so neural responses remain within a finite range. We demonstrate that neural modulation associated with cued reward and punishment in an operant conditioning task, where reward or punishment was delivered according to an individual’s performance, is encoded in cS1, rM1, and PMd. We obtained similar results using either a divisive term based on a combined variable comprised of the cued reward level and a scaled version of the cued punishment level or a function of the brain region’s population activity. Brain regions responded indicating a common driving region or signal led to our results

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