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

Sajad A, Sadeh M, Yan X, Wang H, Crawford JD - eNeuro (2016)

Bottom Line: 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada; Neuroscience Graduate Diploma Program, York University, Toronto, Ontario M3J 1P3, Canada; Department of Biology, York University, Toronto, Ontario M3J 1P3, Canada.

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.

No MeSH data available.


Related in: MedlinePlus

An overview of the experimental paradigm and a conceptual schematic of the possible coding schemes in the FEF. A, Activity was recorded from single neurons in the FEF while monkeys performed a memory-guided gaze task with the head free to move. Monkeys initially fixated a visual stimulus (black dot labeled F) for 400-500 ms. A visual stimulus (black dot labeled T) was then briefly flashed on the screen for 80-100 ms (left). After an instructed delay (variable in duration; 450-850 or 700-1500 ms), the animal made a gaze shift to the remembered location of the target (gray dot labeled T) upon the presentation of the Go-signal. The Go-signal was the disappearance of the initial fixation target (gray dot labeled F). Inaccuracies in behavior were tolerated such that if the final gaze landed within a window around the target, a juice reward was provided. B, Five gaze trajectories to a single target (black circle) within a wide array of targets (5 × 7 for this example session; gray dots) within the approximate RF location of the neuron are shown. Initial fixation positions (tail of the trajectory) were randomly varied within a central zone (large gray circle) on a trial-by-trial basis. Final gaze positions (white circles) fell at variable positions around the target. Variability in initial and final positions (relative to different frames of reference) of target, gaze (i.e., eye in space), eye (in head), and head was used to spatially differentiate sensory and various motor parameters in various frames of reference. We exploited the variability in behavioral errors to differentiate between spatial models based on target position (T) and final gaze position (G). C, Additionally, a continuum of intermediary spatial models spanning T and G were constructed to treat the spatial code as a continuous variable; this allowed us to trace changes in the spatial code as activity evolved from vision to memory delay, during memory delay, and from memory delay to motor. D shows some plausible schemes for the spatiotemporal evolution of a neuronal code based on the following proposed theories: (1) the target code could be transformed into a gaze code early on, and this gaze code maintained during memory (motor theory; light gray line); (2) the target code could be maintained in the memory (sensory theory; black line) and subsequently transformed into a gaze code just before movement initiation; or (3) the spatial code could gradually change from a target code to a gaze code (dark gray line).
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Figure 1: An overview of the experimental paradigm and a conceptual schematic of the possible coding schemes in the FEF. A, Activity was recorded from single neurons in the FEF while monkeys performed a memory-guided gaze task with the head free to move. Monkeys initially fixated a visual stimulus (black dot labeled F) for 400-500 ms. A visual stimulus (black dot labeled T) was then briefly flashed on the screen for 80-100 ms (left). After an instructed delay (variable in duration; 450-850 or 700-1500 ms), the animal made a gaze shift to the remembered location of the target (gray dot labeled T) upon the presentation of the Go-signal. The Go-signal was the disappearance of the initial fixation target (gray dot labeled F). Inaccuracies in behavior were tolerated such that if the final gaze landed within a window around the target, a juice reward was provided. B, Five gaze trajectories to a single target (black circle) within a wide array of targets (5 × 7 for this example session; gray dots) within the approximate RF location of the neuron are shown. Initial fixation positions (tail of the trajectory) were randomly varied within a central zone (large gray circle) on a trial-by-trial basis. Final gaze positions (white circles) fell at variable positions around the target. Variability in initial and final positions (relative to different frames of reference) of target, gaze (i.e., eye in space), eye (in head), and head was used to spatially differentiate sensory and various motor parameters in various frames of reference. We exploited the variability in behavioral errors to differentiate between spatial models based on target position (T) and final gaze position (G). C, Additionally, a continuum of intermediary spatial models spanning T and G were constructed to treat the spatial code as a continuous variable; this allowed us to trace changes in the spatial code as activity evolved from vision to memory delay, during memory delay, and from memory delay to motor. D shows some plausible schemes for the spatiotemporal evolution of a neuronal code based on the following proposed theories: (1) the target code could be transformed into a gaze code early on, and this gaze code maintained during memory (motor theory; light gray line); (2) the target code could be maintained in the memory (sensory theory; black line) and subsequently transformed into a gaze code just before movement initiation; or (3) the spatial code could gradually change from a target code to a gaze code (dark gray line).

Mentions: Assuming that one could track such codes through time, there are several ways that a T–G transition could occur in memory-guided saccades (Fig. 1D). A sustained T code followed by a late T–G transition would be compatible with sensory theories of working memory (Funahashi et al.,1993; Constantinidis et al., 2001), whereas an early T–G transition would be compatible with motor theories of working memory (Gnadt and Andersen, 1988; Gaymard et al., 1999; Rainer et al., 1999; Curtis and D'Esposito, 2006). Alternatively, T–G transition could progressively accumulate during the delay (Gnadt et al., 1991; Wimmer et al., 2014). Another possibility (data not shown) is that there is no transition of coding within any given population of cells, but rather a temporal transition of activity from a T-tuned population of neurons to a G-tuned population (Takeda and Funahashi, 2007).


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

Sajad A, Sadeh M, Yan X, Wang H, Crawford JD - eNeuro (2016)

An overview of the experimental paradigm and a conceptual schematic of the possible coding schemes in the FEF. A, Activity was recorded from single neurons in the FEF while monkeys performed a memory-guided gaze task with the head free to move. Monkeys initially fixated a visual stimulus (black dot labeled F) for 400-500 ms. A visual stimulus (black dot labeled T) was then briefly flashed on the screen for 80-100 ms (left). After an instructed delay (variable in duration; 450-850 or 700-1500 ms), the animal made a gaze shift to the remembered location of the target (gray dot labeled T) upon the presentation of the Go-signal. The Go-signal was the disappearance of the initial fixation target (gray dot labeled F). Inaccuracies in behavior were tolerated such that if the final gaze landed within a window around the target, a juice reward was provided. B, Five gaze trajectories to a single target (black circle) within a wide array of targets (5 × 7 for this example session; gray dots) within the approximate RF location of the neuron are shown. Initial fixation positions (tail of the trajectory) were randomly varied within a central zone (large gray circle) on a trial-by-trial basis. Final gaze positions (white circles) fell at variable positions around the target. Variability in initial and final positions (relative to different frames of reference) of target, gaze (i.e., eye in space), eye (in head), and head was used to spatially differentiate sensory and various motor parameters in various frames of reference. We exploited the variability in behavioral errors to differentiate between spatial models based on target position (T) and final gaze position (G). C, Additionally, a continuum of intermediary spatial models spanning T and G were constructed to treat the spatial code as a continuous variable; this allowed us to trace changes in the spatial code as activity evolved from vision to memory delay, during memory delay, and from memory delay to motor. D shows some plausible schemes for the spatiotemporal evolution of a neuronal code based on the following proposed theories: (1) the target code could be transformed into a gaze code early on, and this gaze code maintained during memory (motor theory; light gray line); (2) the target code could be maintained in the memory (sensory theory; black line) and subsequently transformed into a gaze code just before movement initiation; or (3) the spatial code could gradually change from a target code to a gaze code (dark gray line).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4829728&req=5

Figure 1: An overview of the experimental paradigm and a conceptual schematic of the possible coding schemes in the FEF. A, Activity was recorded from single neurons in the FEF while monkeys performed a memory-guided gaze task with the head free to move. Monkeys initially fixated a visual stimulus (black dot labeled F) for 400-500 ms. A visual stimulus (black dot labeled T) was then briefly flashed on the screen for 80-100 ms (left). After an instructed delay (variable in duration; 450-850 or 700-1500 ms), the animal made a gaze shift to the remembered location of the target (gray dot labeled T) upon the presentation of the Go-signal. The Go-signal was the disappearance of the initial fixation target (gray dot labeled F). Inaccuracies in behavior were tolerated such that if the final gaze landed within a window around the target, a juice reward was provided. B, Five gaze trajectories to a single target (black circle) within a wide array of targets (5 × 7 for this example session; gray dots) within the approximate RF location of the neuron are shown. Initial fixation positions (tail of the trajectory) were randomly varied within a central zone (large gray circle) on a trial-by-trial basis. Final gaze positions (white circles) fell at variable positions around the target. Variability in initial and final positions (relative to different frames of reference) of target, gaze (i.e., eye in space), eye (in head), and head was used to spatially differentiate sensory and various motor parameters in various frames of reference. We exploited the variability in behavioral errors to differentiate between spatial models based on target position (T) and final gaze position (G). C, Additionally, a continuum of intermediary spatial models spanning T and G were constructed to treat the spatial code as a continuous variable; this allowed us to trace changes in the spatial code as activity evolved from vision to memory delay, during memory delay, and from memory delay to motor. D shows some plausible schemes for the spatiotemporal evolution of a neuronal code based on the following proposed theories: (1) the target code could be transformed into a gaze code early on, and this gaze code maintained during memory (motor theory; light gray line); (2) the target code could be maintained in the memory (sensory theory; black line) and subsequently transformed into a gaze code just before movement initiation; or (3) the spatial code could gradually change from a target code to a gaze code (dark gray line).
Mentions: Assuming that one could track such codes through time, there are several ways that a T–G transition could occur in memory-guided saccades (Fig. 1D). A sustained T code followed by a late T–G transition would be compatible with sensory theories of working memory (Funahashi et al.,1993; Constantinidis et al., 2001), whereas an early T–G transition would be compatible with motor theories of working memory (Gnadt and Andersen, 1988; Gaymard et al., 1999; Rainer et al., 1999; Curtis and D'Esposito, 2006). Alternatively, T–G transition could progressively accumulate during the delay (Gnadt et al., 1991; Wimmer et al., 2014). Another possibility (data not shown) is that there is no transition of coding within any given population of cells, but rather a temporal transition of activity from a T-tuned population of neurons to a G-tuned population (Takeda and Funahashi, 2007).

Bottom Line: 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada; Neuroscience Graduate Diploma Program, York University, Toronto, Ontario M3J 1P3, Canada; Department of Biology, York University, Toronto, Ontario M3J 1P3, Canada.

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.

No MeSH data available.


Related in: MedlinePlus