Temporal analysis of reference frames in parietal cortex area 5d during reach planning

Abstract

The neural encoding of spatial and postural reference frames in posterior parietal cortex has traditionally been studied during fixed epochs, but the temporal evolution of these representations (or lack thereof) can provide insight into the underlying computations and functions of this region. Here we present single-unit data recorded from two rhesus macaques during a reach planning task. We found that area 5d coded the position of the hand relative to gaze before presentation of the reach target, but switched to coding the target location relative to hand position soon after target presentation. In the pretarget period the most relevant information for success in the task is the position of the hand relative to gaze; however, after target onset, the most task-relevant spatial relationship is the location of the target relative to the hand. The switch in coding suggests that population activity in area 5d may represent postural and spatial information in the reference frame that is most pertinent at each stage of the task. Moreover, although target-hand coding was dominant from soon after the reach target onset, this representation was not static but built in strength as movement onset approached, which we speculate could reflect a role for this region in building an accurate state estimate for the limb. We conclude that representations in area 5d are more flexible and dynamic than previously reported.

Keywords: monkey; neurophysiology; parietal; reaching; reference frames.

Figure 1.

A, The reference frame reaching task. Gaze fixation (red squares), starting hand position (lower green squares), and targets (upper green squares) were located at −20°, −10°, 0°, or 10° horizontally. B, Coronal fMRI section from monkey G showing the area 5d recording site.

Figure 2.

Example area 5d cell with hand–gaze encoding in the fixation epoch and target–hand coding in the late delay epoch. A, Peristimulus time histograms and raster plots for all 64 conditions. Each subplot shows the response of the neuron to a particular combination of target position and hand position, for all four possible gaze fixation positions. Trials are aligned to movement onset with the dashed lines indicating the mean target onset and go signal, respectively. The shaded regions designate the fixation and late delay epochs. B, Matrices and gradient resultant orientations for the cell shown in A during the fixation (top) and late delay (bottom) epochs.

Figure 3.

Time-step analysis for the example cell shown in Figure 2. Each column shows the response of the cell to a pair of variables (e.g., TG) at each of the four positions for the third variable (e.g., H). In each subplot, the arrows represent the orientation of the matrix gradient resultant calculated for a 200 ms window centered at 100 ms intervals through the trial. Circular plots at the top of each column indicate the appropriate interpretation of arrow direction for each variable pair. Arrow length indicates tuning strength. Data were aligned to target onset (first solid vertical line) for the first 17 time steps and to movement onset (second solid vertical line) for the second 17 time steps, with a short gap indicating the break in alignment. The vertical dashed line indicates the mean go signal and the three shaded boxes at top left show the fixation, early delay, and late delay epochs.

Figure 4.

Time-step analysis for the population of 128 cells showing evolution of reference frames during the task. Columns show the population response to a pair of variables (e.g., TG) at each of the four positions for the third variable (e.g., H). In each subplot, the arrows represent the mean resultant for the population of cells at 100 ms time steps (200 ms window). Circular plots at the top of each column indicate the appropriate interpretation of arrow direction for each variable pair. Arrow length indicates the circular concentration of the matrix gradient orientations and is therefore normalized within each variable pair. Data were aligned to target onset (first solid vertical line) for the first 17 time steps and to movement onset (second solid vertical line) for the second 17 time steps, with a short gap indicating the break in alignment. The vertical dashed line indicates the mean go signal and the three shaded boxes at top left show the fixation, early delay, and late delay epochs.

Figure 5.

Dynamic range distributions by variable pair and epoch. A, Box-and-whisker plots for the full set of dynamic ranges for all cells (top) and only those cells with significant tuning to the variable pair (bottom). In each case, the red line denotes the median, the solid box denotes the 25th and 75th percentiles, and the whiskers extend to the last data point not considered an outlier (open circles). B, Histograms show in more detail the distribution of dynamic ranges for the two main effects reported: HG during the fixation epoch (gray) and TH during the late delay epoch (green). C, Distribution of correlation coefficients from trial-by-trial calculations of the correlation between firing rate and reaction time for individual cell–trial-type combinations.

Figure 6.

Area 5d codes the hand position relative to gaze before target presentation, but codes the reach vector as movement onset approaches. A, Histograms show the distribution of orientations of the matrix gradient resultants and SVD analysis for the population of tuned cells at three epochs during the task (fixation, early delay, and late delay). Each stacked bar represents 22.5° of the circular orientation plot; pale gray indicates separable responses and dark gray indicates inseparable responses. p values show the results of the Rayleigh test for uniformity, corrected for multiple comparisons. B, Histogram for the HG variable pair as described in A, but showing results when trials were collapsed across upcoming target positions (left). Mean gradient resultant orientation when trials were collapsed was −91°; the shaded area represents 95% confidence limits (right).

Figure 7.

Differential recruitment of subpopulations across epochs. Venn diagrams show the numbers of cells significantly tuned to the HG variable pair during the fixation and late delay epochs (A) and to the TH variable pair during the early delay and late delay epochs (B). Some cells were tuned only within a single epoch, whereas others were tuned during both epochs. Histograms show the orientations of the matrix gradient resultants and SVD analysis for each subgroup of cells in the Venn diagram across the specified epochs. Stacked bars represent separable (pale gray) or inseparable (dark gray) responses.