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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

Spatiotemporal progression of neuronal code in VM neurons with sustained delay activity. A shows the results with time-normalized activity sampling, including visual and movement response using the same conventions as in Figure 5B (bottom). B shows the results for only the delay period, with visual and movement responses excluded. Specifically, activity was sampled from 12 half-overlapping steps from the end of the visual response (on average, 266 ms after target onset) until the beginning of the movement response (on average, 85 ms before gaze onset). This duration was on average 635 ms. C shows the spatial code at fixed times intervals relative to the following specific task events: target onset (left); the Go-signal (middle); and gaze onset (right). For target-aligned analysis (C, left), the time from 80 ms after target onset and the earliest Go-signal was divided into eight half-overlapping steps, resulting in a sampling window size fixed for any session but ranging between 80 and 150 ms, depending on whether the earliest Go-signal appeared at 450 or 700 ms relative to target onset for that session. The Go-signal-aligned analysis (C, middle) was performed using 100 ms half-overlapping windows starting at 150 ms before and extending to 150 ms after the Go-signal. The movement-aligned analysis (C, right) was performed using half-overlapping 100 ms sampling windows starting from 150 ms before and extending to 150 ms after gaze onset. Notice that, although there is no change in spatial code triggered by specific task events, there is a progressive change in spatial code from T toward G as we move away from the time of target presentation (left) to the time of gaze onset (right), which is in agreement with the trend seen in A and B.
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Figure 8: Spatiotemporal progression of neuronal code in VM neurons with sustained delay activity. A shows the results with time-normalized activity sampling, including visual and movement response using the same conventions as in Figure 5B (bottom). B shows the results for only the delay period, with visual and movement responses excluded. Specifically, activity was sampled from 12 half-overlapping steps from the end of the visual response (on average, 266 ms after target onset) until the beginning of the movement response (on average, 85 ms before gaze onset). This duration was on average 635 ms. C shows the spatial code at fixed times intervals relative to the following specific task events: target onset (left); the Go-signal (middle); and gaze onset (right). For target-aligned analysis (C, left), the time from 80 ms after target onset and the earliest Go-signal was divided into eight half-overlapping steps, resulting in a sampling window size fixed for any session but ranging between 80 and 150 ms, depending on whether the earliest Go-signal appeared at 450 or 700 ms relative to target onset for that session. The Go-signal-aligned analysis (C, middle) was performed using 100 ms half-overlapping windows starting at 150 ms before and extending to 150 ms after the Go-signal. The movement-aligned analysis (C, right) was performed using half-overlapping 100 ms sampling windows starting from 150 ms before and extending to 150 ms after gaze onset. Notice that, although there is no change in spatial code triggered by specific task events, there is a progressive change in spatial code from T toward G as we move away from the time of target presentation (left) to the time of gaze onset (right), which is in agreement with the trend seen in A and B.

Mentions: Thus, this time-normalization procedure allowed us to consider the entire sequence of visual–memory–motor responses as a continuum. It causes blurring of some other events across trials (e.g., the Go-signal) or mixing of visual and movement responses in the delay period, but these possibilities are controlled for in the Results section (see Fig. 8).


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)

Spatiotemporal progression of neuronal code in VM neurons with sustained delay activity. A shows the results with time-normalized activity sampling, including visual and movement response using the same conventions as in Figure 5B (bottom). B shows the results for only the delay period, with visual and movement responses excluded. Specifically, activity was sampled from 12 half-overlapping steps from the end of the visual response (on average, 266 ms after target onset) until the beginning of the movement response (on average, 85 ms before gaze onset). This duration was on average 635 ms. C shows the spatial code at fixed times intervals relative to the following specific task events: target onset (left); the Go-signal (middle); and gaze onset (right). For target-aligned analysis (C, left), the time from 80 ms after target onset and the earliest Go-signal was divided into eight half-overlapping steps, resulting in a sampling window size fixed for any session but ranging between 80 and 150 ms, depending on whether the earliest Go-signal appeared at 450 or 700 ms relative to target onset for that session. The Go-signal-aligned analysis (C, middle) was performed using 100 ms half-overlapping windows starting at 150 ms before and extending to 150 ms after the Go-signal. The movement-aligned analysis (C, right) was performed using half-overlapping 100 ms sampling windows starting from 150 ms before and extending to 150 ms after gaze onset. Notice that, although there is no change in spatial code triggered by specific task events, there is a progressive change in spatial code from T toward G as we move away from the time of target presentation (left) to the time of gaze onset (right), which is in agreement with the trend seen in A and B.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Spatiotemporal progression of neuronal code in VM neurons with sustained delay activity. A shows the results with time-normalized activity sampling, including visual and movement response using the same conventions as in Figure 5B (bottom). B shows the results for only the delay period, with visual and movement responses excluded. Specifically, activity was sampled from 12 half-overlapping steps from the end of the visual response (on average, 266 ms after target onset) until the beginning of the movement response (on average, 85 ms before gaze onset). This duration was on average 635 ms. C shows the spatial code at fixed times intervals relative to the following specific task events: target onset (left); the Go-signal (middle); and gaze onset (right). For target-aligned analysis (C, left), the time from 80 ms after target onset and the earliest Go-signal was divided into eight half-overlapping steps, resulting in a sampling window size fixed for any session but ranging between 80 and 150 ms, depending on whether the earliest Go-signal appeared at 450 or 700 ms relative to target onset for that session. The Go-signal-aligned analysis (C, middle) was performed using 100 ms half-overlapping windows starting at 150 ms before and extending to 150 ms after the Go-signal. The movement-aligned analysis (C, right) was performed using half-overlapping 100 ms sampling windows starting from 150 ms before and extending to 150 ms after gaze onset. Notice that, although there is no change in spatial code triggered by specific task events, there is a progressive change in spatial code from T toward G as we move away from the time of target presentation (left) to the time of gaze onset (right), which is in agreement with the trend seen in A and B.
Mentions: Thus, this time-normalization procedure allowed us to consider the entire sequence of visual–memory–motor responses as a continuum. It causes blurring of some other events across trials (e.g., the Go-signal) or mixing of visual and movement responses in the delay period, but these possibilities are controlled for in the Results section (see Fig. 8).

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