Transition from Target to Gaze Coding in Primate Frontal Eye Field during Memory Delay and Memory–Motor Transformation

Abstract

The frontal eye fields (FEFs) participate in both working memory and sensorimotor transformations for saccades, but their role in integrating these functions through time remains unclear. Here, we tracked FEF spatial codes through time using a novel analytic method applied to the classic memory-delay saccade task. Three-dimensional recordings of head-unrestrained gaze shifts were made in two monkeys trained to make gaze shifts toward briefly flashed targets after a variable delay (450-1500 ms). A preliminary analysis of visual and motor response fields in 74 FEF neurons eliminated most potential models for spatial coding at the neuron population level, as in our previous study (Sajad et al., 2015). We then focused on the spatiotemporal transition from an eye-centered target code (T; preferred in the visual response) to an eye-centered intended gaze position code (G; preferred in the movement response) during the memory delay interval. We treated neural population codes as a continuous spatiotemporal variable by dividing the space spanning T and G into intermediate T–G models and dividing the task into discrete steps through time. We found that FEF delay activity, especially in visuomovement cells, progressively transitions from T through intermediate T–G codes that approach, but do not reach, G. This was followed by a final discrete transition from these intermediate T–G delay codes to a “pure” G code in movement cells without delay activity. These results demonstrate that FEF activity undergoes a series of sensory–memory–motor transformations, including a dynamically evolving spatial memory signal and an imperfect memory-to-motor transformation.

Decoding Target Distance and Saccade Amplitude from Population Activity in the Macaque Lateral Intraparietal Area (LIP)

“…A number of recent studies have investigated related issues, among them Sereno and Lehky (2011) and two studies by Sajad et al (2015, 2016). Sereno and Lehky have shown that population activity from area LIP allows to decode visual information at high spatial resolution.…”

Integration of eye-centered and landmark-centered codes in frontal eye field gaze responses

“…We began this analysis by considering whether the addition of the landmark (and/or its shift) obviate the basic egocentric target-to-gaze transformation reported in our previous FEF studies (Sajad et al , 2016. Overall, we found that the T and G (in eye coordinates) models continued to dominate visual ( Supplementary Fig.…”

“…Thus, one would expect any cortical signal that integrates egocentric and allocentric information to be present at this point in the system. We recently found that (in the absence of landmarks) the FEF produces a target-to-gaze coding transformation in egocentric coordinates (Sajad et al , 2016. Based on this, one might hypothesize that an allocentric influence should occur within and between these codes.…”

“…In an exhaustive preliminary analysis, we tested if 1) the presence of a visual landmark fundamentally changed the FEF codes reported in our previous studies (Sajad et al , 2016 and 2) if we could narrow the focus of our analysis in the current study. First, we fitted (using Matlab 2015a) visual and motor RFs against the eleven egocentric canonical models ( Supplementary Fig.…”

“…between those canonical types (Fig. 3A, lower left)(DeSouza et al 2011;Sadeh et al 2015;Sajad et al 2015Sajad et al , 2016. Different intermediate model continua were analyzed as in the previous study involving egocentric models and it was revealed that the Te-Ge (Target in eye coordinates to Gaze in eye coordinates) was the most relevant and most of the transformations occurred along this continuum (see results).Based on this previous finding and our preliminary model-fitting analysis (summarized below in the Results section andSupplementary Figures), we retained this continuum (Te to Ge) to quantify the FEF egocentric transformation(Fig.…”