We report the activity of 147 neuronal recordings (78 single and 69 multi-unit) during the aligned target block of the DMS task. A subset of 113 of these neurons was further studied during the orthogonal target block. 18 recordings showed suppression with visual stimulation within the neuronal receptive field (RF) and were excluded from the analysis.
Activity of FEF neurons during the DMS task
The response of a representative example neuron during the object DMS task () is shown in , for samples presented either inside of (Sample In) or opposite (Sample Out) its RF, with the match appearing either inside of (Match In) or opposite (Match Out) the RF. This example neuron illustrates several properties observed in the population response: a visual response to a sample in the RF, sustained delay activity representing the previous sample location, and match location selective activity following target array onset. The visual response to a sample image appearing in the RF was significant whether comparing firing rates from 50-350ms after the sample onset to rates during fixation, or to the same time period on Sample Out trials (both p< 10–7). This sample location selectivity persisted throughout the delay period, with Sample In activity remaining elevated for the period from 250ms after sample offset until 100ms before target onset (Sample In firing rate vs. baseline or vs. Sample Out, both p< 10–7). Following target onset, activity reflected the location of the matching target (Match In vs. Match Out, p< 10–7). Some neurons with no visual response to the sample also exhibited spatially selective delay activity. An example of such a neuron is shown in the bottom panel of . The response of this neuron did not change from baseline when the sample appeared in the RF (Sample In visual response vs. baseline, p =0.730). However, after sample offset, the neuron's response increased and remained elevated in a manner dependent on prior sample location (Sample In delay response vs. baseline, p< 10–7; Sample In vs. Sample Out, p< 10–7).
The normalized response of a population of 129 FEF neuronal recordings is shown in . As expected, FEF neurons showed selectivity for the location of the sample during its presentation. More importantly, the sample location selectivity persisted throughout the delay period. The distributions of population AROC areas during different task epochs, reflecting the ability of neurons to discriminate between different sample locations and sample objects, are shown in -D. Both object and location information were greatest during the sample period ([ROCsample –ROCdelay]; location = 0.153, p< 10–7; object = 0.049, p =0.0220), but significant selectivity for these properties persisted during the delay period (location ROCdelay=0.580, p<10–7; object ROCdelay=0.506, p =0.031). Although there was object selectivity during the delay period, both the magnitude of that selectivity and the proportion of neurons with significant selectivity were less than those for location selectivity during the same period (99 location-selective neurons vs. 29 object selective neurons, Fisher's exact test p< 10–7; object ROCdelay vs location ROCdelay p< 10–7). Delay period location selectivity was not significantly different for cells with and without a visual response (p = 0.736). Following target array onset, FEF activity reflected both the matching target location (location ROCtarget=0.544, p =7.46×10-4) and target identity (object ROCtarget=0.544, p =1.35×10-4).
Fig 2 FEF population selectivity for sample location and object identity. A) The mean normalized response of FEF neurons (n=129) to samples presented inside (greens) or opposite (blues) the FEF RF, when the matching target appeared inside (light green, cyan) (more ...)
Delay period activity during the orthogonal targets block
The relative positions of sample and target stimuli during the orthogonal block, in which the target positions were rotated 90° with respect to the FEF RF, are shown in . The activity of an example neuron during the aligned and orthogonal blocks is shown in . As expected given the change in target position, activity during the target period was greatly reduced in the orthogonal block (p<10–7). The critical question was whether the delay period activity would be affected by the change in target position: it was not. The delay period activity of this example neuron did not significantly change between blocks (p = 0.699). The population response during aligned and orthogonal target blocks is shown in (n=95). As expected, responses to the targets were significantly reduced in the orthogonal block, both for Match In/Ipsi trials (; aligned block = 0.553, orthogonal block = 0.171, p<10–7) and for Match Out/Contra trials (aligned block 0.462, orthogonal block = 0.235, p<10–7). However, delay period selectivity across the population, measured with a location selectivity index (SI), was not significantly different between the aligned and orthogonal target blocks (), either for the population as a whole (p = 0.812), or considering only neurons with significant delay selectivity (n=64, p = 0.961). Restricting the delay period analysis to neurons with a significant change in target period activity between blocks also did not yield a difference in delay period selectivity (n=80, Sample In, p = 0.465; SI, p = 0.775). We considered that if delay period activity reflects anticipation of the target array, then the change in Sample In activity during the delay period should correlate with the change in target period response for each recording. However, a comparison between blocks revealed that the fractional change in Sample In firing rate was significantly greater during the target period than during the delay period (; log(aligned/orthogonal), target period = 0.390, delay period = -5.10×10–3, target vs. delay, p< 10–7). The fractional change in activity between aligned and orthogonal blocks was still significantly larger during the target period than during the delay period when limiting the analysis to neurons with significant delay period selectivity (log(aligned/orthogonal), delay period = -0.0119, target period, 0.370; target vs. delay, p< 10–7). Thus, delay period activity reflected sample location independent of the upcoming target array position.
Fig 3 The activity of an example FEF neuron during the aligned and orthogonal blocks. A) Object DMS task, orthogonal target positions: the match and nonmatch images appear at locations rotated 90° from the FEF RF. B) Top panel, the response of an example (more ...)
Fig 4 Delay period selectivity was unaltered by change in target positions. A) The response of FEF neurons (n=95) during the aligned block (top) and the orthogonal block (bottom). Conventions are as in . B) Target period responses were reduced in the (more ...)
Delay period selectivity was statistically identical between aligned and orthogonal blocks. However, within a brief window prior to target onset FEF activity reflected the location of the upcoming target array. This ‘pre-target’ period began 100ms prior to target onset and continued until the onset of the earliest visual response (50ms after target onset). As shown in , during the pre-target period there was increased activity in the aligned block as compared to the orthogonal block. This target position dependent difference in activity was observed regardless of prior sample location (aligned vs. orthogonal block, Sample In p = 1.61×10–5; Sample Out p = 0.0013; average across sample positions shown in 5B). We examined the magnitude of this pre-target activity over the time-course of the aligned and orthogonal blocks to see whether it was affected by familiarity with the target locations. An ANOVA comparing pre-target activity across trials within a block showed a significant effect of neuron and aligned vs. orthogonal block (p< 10–7), but not of trial (p = 0.885). Furthermore, a significant effect of target position on pre-target period firing rates was detected within the first ten trials of each block (p = 0.0407), suggesting that monkeys quickly transitioned between the target position expectations of the two blocks. Delay period selectivity was likewise present in these early trials within a block, and statistically indistinguishable from that seen in the remainder of the block (delay SI for first 20 trials vs remainder, orthogonal block p = 0.911, aligned block p = 0.588).
Fig 5 Pre-target activity anticipates target positions. A) Pre-target activity of FEF neurons during the aligned (green, blue) and orthogonal (red, yellow) blocks, when the sample appeared inside (green, red) or opposite (blue, yellow) the FEF RF. Black bar (more ...)
Delay period and target selectivity on error trials
The delay period selectivity observed in both the aligned and orthogonal target blocks varied with performance. Overall, there was higher delay period selectivity on error trials than on correct trials (). Using recordings with at least five incorrect trials of each type, delay SIs were found to be significantly larger on error trials, both for the aligned block (; n=109, p =1.57×10-3; n=76 with paired orthogonal recordings, p = 2.91×10-3) and the orthogonal block (; n=83, p = 5.23×10-3). The magnitude of the difference in SIs between correct and error trials did not significantly differ for the aligned vs. orthogonal block, either for the population as a whole (n=76 neurons with sufficient incorrect trials in both blocks; change in SI, correct – incorrect, aligned block = -0.0173, orthogonal block = -0.0188, p = 0.864), or for neurons with significant delay selectivity (n=51, p = 0.708). No such reduction in SI was observed during the visual responses (orthogonal block, p = 0.482; aligned block, p = 0.125). In the aligned block, target period activity often reflected target location (as shown in ). We examined the target location selectivity of the FEF for correct vs. error trials, where target selectivity on error trials indicates higher activity when the matching target appears in the RF (as opposed to indicating the direction of the saccade). We found that target selectivity across the population was the same for error trials (; n=103 neurons recorded during experiments with sufficient incorrect trials to perform analysis, p =0.265; n=85 neurons with significant target location selectivity, p =0.731). Pre-target anticipatory activity was likewise unaltered on error trials ([aligned – orthogonal] for correct trials vs. incorrect trials, Sample In p = 0.804, Sample Out p = 0.959). Despite the irrelevance of sample location to task performance, sample location information was maintained throughout the delay period, and the magnitude of that spatially selective delay activity was correlated with performance in both the aligned and orthogonal versions of the task.
Fig 6 Delay (A,B) and target (C) activity on correct vs. incorrect trials. A) Delay selectivity indices (SIs) were larger on incorrect trials for the aligned block (n=109). B) Delay SIs were larger on incorrect trials for the orthogonal block (n=83). Neurons (more ...)