Landmark-Centered Coding in Frontal Cortex Visual Responses

Adrian Schütz,Frank Bremmer,Hongying Wang,Xiaogang Yan,Vishal Bharmauria,John Douglas Crawford

doi:10.2139/ssrn.3733983

Adrian Schütz, Frank Bremmer + Show 4 more

Open Access

https://doi.org/10.2139/ssrn.3733983

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Abstract

Visual landmarks influence spatial cognition, navigation and goal-directed behavior, but their influence on visual coding in sensorimotor systems is poorly understood. We hypothesized that visual responses in frontal cortex gaze control areas encode potential targets in an intermediate gaze-centered / landmark-centered reference frame that might depend on specific target-landmark configurations rather than a global mechanism. We tested this hypothesis by recording neural activity in the frontal eye fields (FEF) and supplementary eye fields (SEF) while head-unrestrained macaques engaged in a memory-delay gaze task. Visual response fields (the area of visual space where targets modulate activity) were tested for each neuron in the presence of a background landmark placed at one of four oblique configurations relative to the target stimulus. 102 of 312 FEF and 43 of 256 SEF neurons showed spatially tuned response fields in this task. We then fit these data against a mathematical continuum between a gaze-centered model and a landmark-centered model. When we pooled data across the entire dataset for each neuron, our response field fits did not deviate significantly from the gaze-centered model. However, when we fit response fields separately for each target-landmark configuration, the best fits shifted (mean 37% / 40%) toward landmark-centered coding in FEF / SEF respectively. This confirmed an intermediate gaze / landmark-centered mechanism dependent on local (configuration-dependent) interactions. Overall, these data show that external landmarks influence prefrontal visual responses, likely helping to stabilize gaze goals in the presence of variable eye and head orientations.

Highlights

In daily life, we implicitly or explicitly use visual landmarks for navigation and goal-directed behavior [1,2,3]
We found no significant shift toward the landmark (TL) in the pooled analysis, i.e., the visual response was best described by the to fixation (TF) model
Our analysis shows that visual landmarks can influence the visual code in both the from neurons in the frontal (FEF) and the supplementary eye field (SEF)

Summary

Introduction

We implicitly or explicitly use visual landmarks for navigation and goal-directed behavior [1,2,3]. To generate a reach command for a coffee mug on a table, the brain might initially code the location of the mug relative to the eye, but other cues such as edges of the table or a nearby book may modulate these codes before they are converted into shoulder-centered reach commands 5. To date such influences have been observed in the brain’s memory and motor codes [6,7,8] but it is unclear how these signals are multiplexed in the sensory inputs to these systems. Human studies have suggested that egocentric and allocentric visual codes are separated in the dorsal and ventral visual streams, respectively [14,15,16] and converge in the frontal cortex for action 8, but again, the mechanisms are unknown

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