Sensorimotor transformation elicits systematic patterns of activity along the dorsoventral extent of the superior colliculus in the macaque monkey

Corentin Massot,Uday K Jagadisan,Neeraj J Gandhi

doi:10.1038/s42003-019-0527-y

Corentin Massot, Uday K Jagadisan + Show 1 more

Open Access

https://doi.org/10.1038/s42003-019-0527-y

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Abstract

The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. To date, the spatial and temporal properties of population activity along its dorsoventral axis have been inferred from single electrode studies. Here, we recorded SC population activity in non-human primates using a linear multi-contact array during delayed saccade tasks. We show that during the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. During the delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ~ 100 ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ~ 28 ms before saccade onset. Collectively, these results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze.

Highlights

The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations
Multi-unit spiking activity (MUA) and local field potentials (LFPs) were recorded on each contact of a 16-channel laminar probe that spanned the dorsoventral extent of the SC in two Rhesus monkeys performing visually guided (VG) and memory-guided (MG) delayed saccade tasks (Fig. 1)
Spike density functions aligned on visual burst and saccade onsets for an individual session of VG trials are shown in Fig. 2a, b

Summary

Introduction

The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ~ 28 ms before saccade onset These results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze. Linear microelectrodes have recently been used for such structure-to-function mapping, in cortical regions, since they enable the simultaneous measurement of neural activity across multiple layers This approach has provided insights into how sensory[8,9,10,11] and cognitive processes like spatial attention[12,13], working memory[14], decision-making[15], and episodic encoding[16] are mediated as a function of depth, as well as about modes of communication between layers in driven and quiescent states[17,18]. We present these results in the context of other studies of functional organization and discuss the potential implications of a structure-to-function mapping for sensorimotor transformations

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