Examples of SP × location interaction neurons: tuning to a previous stimulus. A, Histograms of activity and tuning curves from a motor cortex neuron that had a significant SP × location interaction for list length 3 trials in the ANCOVA (F(14,211) = 2/73, p = 0/001). Histograms represent cell activity during 8 sequences of list length 3. This neuron had a significant directional tuning during the third SP epoch (blackened in the histograms). However, the tuning was not with respect to the current (third) stimulus but rather to the stimulus that was presented in the previous (second) SP epoch. Thus, the left histograms are ordered with respect to the second stimulus (numbers in bold font). This tuning toward the second stimulus is seen in the bottom left tuning curve (preferred direction of second stimulus during epoch 3 = 157 degrees, bootstrap p < 0/001). The histograms on the right (middle of page) show the same data, but now ordered with respect to the third stimulus (bold font). The plot below shows mean cell activity (±SD) in the third SP epoch with respect to the location of the third stimulus. There was no significant directional tuning to the current (third) stimulus, as evidenced by this plot and the directional analyses (bootstrap p > 0/05). B, Example of a prefrontal neuron with a significant SP × location interaction in the ANCOVA for list length 4 (F(21,443) = 2/51, p < 0/001).
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We examined more closely the activity of these neurons by analyzing the directional effect during each SP epoch of the list presentation. More specifically, we sought to explore whether the activity during a given epoch was spatially tuned and, if so, whether the activity was tuned to the current stimulus or to a stimulus presented previously during the list presentation. To this end, we computed the mean resultant of the epoch activity associated with the current stimulus and the mean resultant of the same activity associated with the direction of the stimuli presented in the previous epochs. Then, we selected the greatest mean resultant and tested its statistical significance using the bootstrap procedure (1000 bootstraps).
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Here we compare activity during sequence presentation among three areas: primary motor, premotor, and dorsolateral prefrontal cortex. We also report neurophysiological evidence supporting a relative, as opposed to absolute, coding of serial (https://yamamotonight-m.ru/content/uploads/files/download/split-second-velocity-serial-keygen.zip) order.
The animals were 2 male rhesus monkeys (Macaca mulatta, 6–8 kg body weight). They are referred to as Monkey 1 and Monkey 2. Care and treatment of the animals during all stages of the experiments conformed to the guidelines described in the Guide for the care and use of laboratory animals (National Research Council, 1996). The animal protocol was approved by the respective Institutional Animal Care and Use Committees of the Minneapolis Veterans Affairs Medical Center and of the University of Minnesota.
Many neurons in all cortical areas sampled showed modulation of spike activity during the memory scanning task. This modulation occurred during the list presentation period and/or during the response period. Examples of neuronal activity during the memory scanning task are presented in Figure 2. The activity of two neurons from each cortical area is illustrated. Each raster plot shows the spiking activity of one neuron during five repetitions of one condition, where a condition represents the combination of list length, sequence, and SP of the test stimulus. The histogram represents the average time-varying neuronal activity. It can be seen that the modulation of activity during the list presentation period (when the monkey was making no limb movement) was often similar to, or even greater than, the modulation during the response period. The analyses presented in the following sections explore in more detail the neuronal activity during the list presentation period and how it was affected by the factors defining the sequence of stimuli.
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Instead, eye fixations by this monkey were often made to the current stimulus; this was the most frequent for the first stimulus and less so for the following ones. Similar to Monkey 1, during the last epoch of the list presentation, Monkey 2 looked preferentially to one of the stimuli in the middle of the sequence. Eye fixations to the middle stimuli started even during the penultimate epoch for list lengths of four and five stimuli.
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We compared the two correlations for each pair of list lengths and for each cortical area. In all cases, we found that the correlations based on a relative time-varying pattern of activity were higher than the correlations of activity in actual time. However, the most informative of these analyses is the one comparing the patterns of activity during sequences of three and five stimuli. In this case, the difference between the actual and the relative time scale is the greatest; therefore, the possibility of discrimination between the two hypotheses is the most favorable. The results of this analysis are presented in Figure 9B and Table 4. Figure 9B plots the correlation of activity in actual time against the correlation of activity in relative time for motor cortical neurons. The distribution for each type of correlation is illustrated in the margins of the scatterplot in the same figure. The distribution of correlations based on relative time were more skewed toward higher values than the correlations based on actual time. Table 4 shows the average correlations, calculated using Fisher's z transformation (Snedecor and Cochran, 1989), for each cortical area. The correlation coefficients based on a relative time scale were significantly higher than those based on actual time in each cortical area investigated.
The analyses discussed above indicate that neural activity during the list presentation period often varied with sequence parameters (SP and location). Thus, it is possible that these neurons were contributing to the neural encoding of the sequence.
While the monkeys had to maintain the cursor within the center-hold window during list presentation, small movements within that window were possible. For this reason, we tested for possible modulation of EMG activity during the list presentation period by performing the same main ANCOVA on the rectified EMG as the one performed on the neuronal activity. For both monkeys, the majority of muscles did not show any significant effect of the list presentation factors, although a few muscles did show significant effects. The number of muscles in each category of ANCOVA effects is presented in Table 7.
Bottom, SP × location interaction. The middle of each bubble is the penetration site, and the diameter of each bubble represents the percentage of each combination of neuron and list length that showed significant effects in the ANCOVA (as per the scale on the right of the figure). Data from both monkeys were pooled into a common coordinate frame, and the location of the central sulcus, superior precentral sulcus, arcuate sulcus, and principal sulcus in this common frame is drawn in gray for each of the effects. Dashed line indicates the border between motor and premotor cortex. Top left, Dashed rectangle represents the approximate brain region covered by each plot. The proportions refer to the absolute prevalence of each significant effect, regardless of what other effects attained significance (see Results). CS, Central sulcus; SPS, superior precentral sulcus; AS, arcuate sulcus; PS, principal sulcus.
All neurons in the last group were tuned during multiple epochs but, unlike neurons in category 4, they were tuned to different stimuli across epochs. The proportion of neurons in each of these categories is indicated in Table 3 for each cortical area and each list length. We found that many interaction neurons had a significant directional tuning to the current or a previous stimulus in only one epoch of the list presentation period. Remarkably, the proportion of neurons directionally tuned to a previous stimulus was higher than that of neurons tuned to the current stimulus.
EMG activity during task performance was recorded with intramuscular, multistranded, Teflon-coated wire electrodes (Schwartz et al, 1988). The EMG recordings were made during separate sessions from the neural recordings.
As shown above, many neurons in each of the cortical areas investigated showed significant effects of the sequence parameters (SP, location, or their interaction) during the list presentation period. However, neurons in each of the three areas are also known to have directionally selective activity during arm movements to targets in 2D space (Georgopoulos et al, 1982; Weinrich et al, 1984; di Pellegrino and Wise, 1993).
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Comparing the neural activity profile across list lengths: actual versus relative time. A, Examples of one neuron from each cortical area. Plots of time-varying neuronal activity during the list presentation of 3 and 5 stimuli in either an actual (left plots) or a relative (right plots) time scale. Gray line indicates the mean activity profile during list length 3 trials. Black line indicates the mean activity profile during list length 5 trials. For each plot, activity is scaled between its minimum and its maximum activity. Plots in left column represent cell activity in actual time, and the abscissa is scaled in milliseconds. Vertical dotted lines indicate the onset of each list stimulus and of the test stimulus. Plots on right represent neural activity during each list length on the same (relative) time scale, and the abscissa is unit-less. The patterns of activity were better correlated in the relative time scale than in the actual time scale, as visualized by the better matching of the curves and by the correlation coefficients listed above each plot.
To further compare the neuronal activity during list presentation with that during the movement, we selected cells with significant directional tuning during both periods and calculated the circular correlation of the two preferred directions. For this analysis, we selected neurons with a significant SP × location interaction in the ANCOVA, which were directionally tuned in only one epoch during list presentation (Table 3) and also displayed directional tuning during the response. The results are presented in Table 5. Overall, there was no systematic relation between the preferred directions during the list presentation and during the response in motor and premotor cortex. The circular correlations were higher in the few prefrontal cells that were directionally tuned in both periods (although they did not reach statistical significance).
In the raster displays, each line indicates one trial. Small tick marks indicate action potentials. Each line also has 6 large tick marks, which indicate the following (in order): the beginning of the center hold period, the start of the list presentation period, the onset of the test stimulus, the beginning of the movement, the end of the movement, and 500 ms after the end of the movement. The rasters are aligned to the presentation of the test stimulus. The vertical lines on the histograms indicate the following (in order): the onset of each list stimulus, the onset of the test stimulus, the mean onset time of the movement, and the mean end time of the movement. Each histogram bar represents the mean cell discharge rate in a 50 ms bin. Neuronal activity was modulated during the list presentation (when no limb movement occurs), as well as during the response. Top right, The list presentation period, test stimulus onset, and movement periods are labelled.
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In essence, this analysis evaluates how well the pattern of activity (across multiple neurons) during a given SP epoch can be distinguished from the pattern of the same ensemble during other SP epochs. At the level of a single sequence, each sequence element is uniquely identified by both its SP and its location. For example, for a sequence of 90-270-45, identifying a sequence element as “270” or “the second stimulus” is equivalent. The discriminant analysis was applied using each sequence separately, and the resulting classification rates were averaged across sequences, and thus indicated how accurately the individual sequence elements were classified (as opposed to SP or location per se). Because all neurons were included in this analysis, and the most common significant effects in the main ANCOVA were SP and SP × location interaction, activity relating to both factors likely contributes to the classification.
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Significant effects of sequence parameters were more common than significant effects of movement direction in the premotor and prefrontal areas, whereas the two types of effects were about equally prevalent in the motor cortex. Overall, motor cortex had the highest proportion of cells that was exclusively related to movement, prefrontal cortex had the highest proportion exclusively related to sequence parameters, and premotor cortex had the highest proportion related to both. In all areas, a large proportion of cells that had directionally selective activity during the movement also had a significant relation to sequence parameters during the list presentation period. That is, these neurons were remarkably protean, coding for different aspects of the task during different periods of the trial.
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Gaze direction data from Monkey 1 were obtained in separate sessions from the neural recordings. For Monkey 2, gaze direction was recorded simultaneously with the neural recordings, using either the infrared oculometer or a scleral search coil system (Fuchs and Robinson, 1966; Judge et al, 1980). A calibration procedure was performed before the recording sessions by having the monkey fixate a series of targets on the screen. Eye position was sampled at 500 Hz for Monkey 1 and 200 Hz for Monkey 2.
In all three cortical areas, neurons with a significant main effect of stimulus location were rare. At first glance, this may appear surprising given the well-known directional coding of delay-period activity in all three cortical areas (Funahashi et al, 1989; Georgopoulos et al, 1989; di Pellegrino and Wise, 1993). This lack of location effects implies that the neural representation of the sequence was not accomplished by sequentially activating populations of neurons that encode stimulus location. However, because the stimuli remained on the screen throughout the trials, the stimulus locations did not need to be held in memory. Rather, it was the serial order of the stimuli that had to be retained to perform the task, and neurons with a significant effect of SP were common in all three areas.
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We tested the effect of the direction of saccade by analyzing the neuronal activity preceding saccades in different directions. Saccades had to be preceded and followed by a 250 and 100 ms fixation period, respectively, to be included in the analysis. In addition, they had to be restricted within a 7 degree radius disc centered on the middle of the screen, and had to have an amplitude >3 degrees. The presaccadic activity was computed as the mean discharge rate in a 100 ms period preceding the saccade onset. The discharge rates were grouped according to the direction of the saccade in 45 degree bins. Because saccades in different directions could start from different locations, we controlled for the possible effect of gaze direction on the presaccadic activity. To this end, we used the discharge rate in a 50 ms control period starting 200 ms before the saccade as a covariate in the ANCOVA, with direction of saccade as factor.
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For Monkey 1, we selected 16 sequences of three stimuli and 4 sequences of four stimuli to be used during the neuronal recording sessions. These sequences were the same in each experimental session. Within each list length block, the sequence and SP of the test stimulus for each trial were selected at random until one correct response to each instance was made. This was repeated until 5 correct responses were made to each combination of sequence and SP of the test stimulus. Thus, to complete a block of sequences of three or four stimuli, Monkey 1 needed to perform 160 or 60 trials, respectively (number of trials = number of sequences × number of SPs of the test stimulus × 5 repetitions). For Monkey 2, the experimental sessions included up to three blocks of sequences of three, four, and five stimuli, respectively. Each block was composed of 8 different sequences of stimuli. These sequences varied in each experimental session. One sequence in each block was taken from a fixed pool of two possible sequences. The remaining 7 sequences were randomly generated under the constraint that each possible stimulus location was equally represented in each SP during the experimental session.
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Collective is a synth plugin that also includes many sampled sound sources. It easily covers the basics of the virtual analog world and includes four oscillators, multiple sound layers per preset, several filter types, LFOs, envelopes, four-operator FM, four-band EQ, effects, and over 600 presets. Expansion packs are also available on the Tracktion website. The samples within Collective are from Klaus Peter Rausch’s own collection. He has worked with many leading companies such as Korg, Yamaha and Alesis over the past few decades.
Next, we explored this relative coding of SP at the neuronal ensemble level. Figure 10 shows raster plots of each trial of the memory scanning task with list lengths 3, 4, and 5, from an ensemble of 13 simultaneously recorded motor cortical neurons. Each line represents one trial, and each of the 13 cells is plotted in a different color. All sequences are shown, randomly intermixed within each list length.
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In summary, these results show that, at the end of the list presentation period, both monkeys directed their gaze toward a stimulus that was in the middle of the sequence presented. This preferential pattern of gaze direction was related to the serial order of the stimulus, and not to its spatial location.
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We examined the cortical distribution of neurons whose activity was significantly related to sequence parameters. Figure 4 shows the distribution of effects found in the main ANCOVA with respect to the recording sites. The electrode penetration sites from both monkeys were combined in a common coordinate frame, and the approximate locations of anatomical landmarks are displayed in gray. The “bubbles” on the plot represent the proportion of cases that had a significant effect in the main ANCOVA. A case represents the combination of neuron and list length. For example, if two neurons were recorded at a given penetration site and both showed a significant SP effect in all list lengths of the memory scanning task, then the size (diameter) of the bubble indicates that 100% of the cases showed an SP effect. If only one cell was recorded at a given site, and it showed an SP effect in list length 3 and 4 but not list length 5, the size of the bubble would indicate 66/7% of cases with an SP effect. The proportion of cases with a significant effect of SP, location, and SP × location interaction is plotted from top to bottom, respectively. In this analysis, the proportions represent the absolute prevalence of each effect, and a main effect of SP or location is not ignored if a significant interaction is also present (see Neuronal activity associated with list presentation factors). This provides a more detailed picture of how these effects were distributed in the frontal cortex.
Also, they can’t be easily re-arranged in a different order. The only way to do that is to select the other effect type you want in whichever effect bay(s).
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Figure 4 suggests that the distribution of the significant effects was not uniform across the brain regions sampled. We used logistic regression to assess whether the x and/or y coordinate of each penetration site affected the likelihood of a significant ANCOVA effect. In precentral (motor plus premotor) cortex, the likelihood of an SP effect increased with increasing (anterior) distance from the central sulcus, whereas in prefrontal cortex an SP effect was less likely with greater dorsal distance from the principal sulcus.
To quantify this observation, we calculated two sets of correlations between the time series of activity for sequences of a given list length with the time series of activity in a different list length. The first correlation evaluated the similarity in actual time of the activity profiles in different list length conditions. Therefore, the length of the time series used in this analysis was limited to the length of the shortest list length selected for the comparison, to compare only common SP epochs. For example, to compute the correlation of the time-varying activity during sequences of three and five stimuli, we used the activity recorded during the list presentation of the first three stimuli in both list length conditions. The correlation of activity in actual time tested how similar the patterns of activity were across common SP epochs for different list lengths.
Prevalence of significant gaze direction effects among neurons with significant sequence parameter effects. For each cortical area, bars represent the proportion of neurons with a significant gaze direction effect among those that had (1) no significant effects in the main ANCOVA (None), (2) a significant effect of SP but not location or SP × location interaction (SP), or (3) a significant SP × location interaction. The other two categories from the main ANCOVA (location main effect only, or main effects of both SP and location) were excluded because very few neurons fell into these categories. Error bars indicate mean ± SD proportion, averaged across list length. For each category of sequence parameter effects and for all cortical areas, only a minority of neurons had gaze-related activity.
Relative coding of SP: ensemble of 13 simultaneously recorded neurons. The neural activity of a simultaneously recorded ensemble is plotted as rasters. Data are from Monkey 2, motor cortex, during the list presentation period of the memory scanning task with list length 3 (top), 4 (middle), and 5 (bottom). The spikes from each of the 13 neurons in the ensemble are plotted with a different color. The spikes were plotted thicker than in previous raster plots, to aid the discrimination of the different colors.
Table 1 reports the number of neurons that were isolated in each cortical area. In addition, the table indicates the number of neurons that were recorded across different list length conditions in the memory scanning task. Most neurons were recorded during multiple blocks of different list length. Although we tried to record each neuron in all conditions, this was not always possible because of the duration of the experimental sessions. Data from Monkey 1 during the response period (Pellizzer et al, 1995) and some aspects of motor cortex data from both monkeys during list presentation (Carpenter et al, 1999) have been presented previously.