Local Neural Processing and the Generation of Dynamic Motor Commands within the Saccadic Premotor Network

Characteristics of LFPs recorded from typical OPN. A, Example traces of horizontal eye velocity, LFP recording, and spiking activity. Note that, regardless of direction, whenever a saccade is made there is a pause in the unit activity and a deflection in the LFP trace that is consistent with a net hyperpolarization. B, A raster displaying spiking activity, as well as average LFP, eye velocity, and eye position traces, is shown for both ipsilateral (left) and contralateral (right) directed saccades. C, D, Plots of LFP duration versus saccade duration (C) and LFP time integral versus saccade amplitude (D) for both ipsilateral (left) and contralateral (right) directed saccades. E, The LFP profile (not inverted) matched eye velocity (superimposed on the LFP trace for comparison) during a typical (left panel) and an atypical (e.g., complex temporal dynamics; right panel) saccade. The timing and amplitude of the peaks in the velocity and LFP profiles are almost synchronous. Inset shows the lead time of the LFP and firing rate responses relative to eye velocity. *Additional examples are illustrated in supplemental Figure 2 (available at www.jneurosci.org as supplemental material).

Characteristics of LFPs recorded from typical SBN. A, Example traces of horizontal eye velocity, LFP recording, and single-unit activity. Note that whenever a saccade is made in the cell's preferred direction, an LFP response that is consistent with a net depolarization occurs, whereas when the saccade is in the antipreferred direction, the response is consistent with a net hyperpolarization. B, The LFP profile matched eye velocity during typical (left panel) and atypical (e.g., complex temporal dynamics; right panel) saccades. The timing and amplitude of the peaks in the velocity and LFP profiles are almost synchronous. Inset shows the lead time of the LFP and firing rate responses relative to eye velocity. *Additional examples are illustrated in supplemental Figure 2 (available at www.jneurosci.org as supplemental material). C, A raster displaying unit activity, as well as average LFP, eye velocity, and eye position traces, is shown in the preferred (C1) and nonpreferred (C2) directions.

Dynamic analysis of LFP and single unit responses recorded from an example SBN, MN, and OPN. A1–A3, The fits (red traces) obtained using Equation 1 (SBN and OPN) or Equation 2 (MN) (see Materials and Methods for details) are superimposed on the LFP trace (gray trace, third row) and spiking activity (gray filled profile, fourth row) for the neuron's preferred (left panels) and nonpreferred (right panels) directions. Both the firing rate and LFPs encoded eye velocity in the preferred direction. In contrast, in the neuron's nonpreferred direction, eye velocity was well encoded by LFPs, but not by spiking activity. Insets show the eye velocity coefficient obtained using Equation 1 (SBNs and OPNs) or Equation 2 (MNs) for both ipsilateral and contralateral saccades. Note that the VAF values were always calculated when fitting the entire dataset of saccades. B1–B3, Histograms of VAFs estimated for LFPs during ipsilateral (i.e., preferred) and contralateral (i.e., nonpreferred) saccades for each population of neurons recorded.

Stimulus reconstruction of the eye velocity using LFPs and spikes recorded from SBN neuron. Eye velocity (black trace; duplicate for clarity in first and second row), stimulus reconstruction of eye velocity using LFPs (first row; blue trace) or spikes (second row; red trace), LFPs, and spiking activity are shown for saccades made in the preferred (A) and nonpreferred (B) directions. Note that in the preferred direction, both the LFPs and spikes were able to accurately reconstruct the corresponding eye velocity signal (CF_LFP = 0.56; CF_spike = 0.49). In the nonpreferred direction, however, only the LFPs precisely described the eye velocity (CF_LFP = 0.55; CF_spike = 0). Notably, the CFs were calculated for the entire signal length, which was made up of at least 40 saccades. Optimal filters were calculated for each individual neuron. The insets show the mean optimal filter estimated from LFPs for the reconstructions of the eye velocity profiles for the population of neurons.

Average population coding fractions for MNs (A), SBNs (B), and OPNs (C) when the reconstruction of the eye velocity was applied with the LFP signal (gray), spike train (white), and firing rate (black). Note that LFPs recorded from MNs, SBNs, and OPNs are able to reconstruct the eye velocity in both the neurons' preferred (i.e., ipsilateral) and nonpreferred (i.e., contralateral) directions. Although the spike train and firing rate accurately reconstruct the eye velocity in the preferred direction of the MNs and SBNs, these signals fail to do so in the neurons' nonpreferred direction. C, Spiking activity and firing rate recorded from OPNs were unable to reconstruct the eye velocity in both the ipsilateral and contralateral directions.

STA and SFC for MNs (left column) and SBNs (right column). A1 and B1 show the STAs of 2 example cells centered on the first spike of each trial. The onset of the first 2 standard deviation threshold crossing in the STA was computed 120 to 40 ms preceding spike onset (see gray areas). The latency was obtained by measuring the duration between the spike onset and the STA onset (see vertical arrow). For both example neurons, the STA onset precedes the onset of spiking activity. A2 and B2 show population averages of STA superimposed on ±1 SEM (gray area). On average, the STA onset precedes the onset of spiking activity. The insets show the average SFC computed by taking the maximum of the normalized power spectrum for each neuron. Both classes of neurons display high SFCs indicating a strong positive correlation between the LFP signals and the spiking activity.

Spatial relationship of SBN LFP responses. A, Spiking activity and average LFPs recorded simultaneously from a typical SBN during saccades, of equal amplitude (10 deg), made in 8 different directions (e.g., left, right, up, down, and oblique) are superimposed on average spectrograms. Zero and one hundred eighty degrees correspond to the cell's preferred and antipreferred directions, respectively; 90 and 270 deg correspond to vertical up and vertical down saccades, respectively. The x- and y-axes represent time and frequency, respectively, while LFP power is color coded. B, Plot of saccade endpoint relative to the origin where the x- and y-axes represent horizontal and vertical components, respectively, and the time integral taken over the saccade interval of the corresponding LFP response is color coded. Left and right insets show tuning curves for saccades (5 to 10 deg) made in contralateral and ipsilateral directions, respectively.

Spatial relationship of OPN LFP responses. A, Spiking activity and average LFPs recorded simultaneously from a typical OPN during saccades, of equal amplitude, made in 8 different directions (e.g., left, right, up, down, and oblique) are superimposed on average spectrograms. Zero and one hundred eighty degrees correspond to the cell's ipsilateral and contralateral directions, respectively. The x- and y-axes represent time and frequency, respectively, while LFP power is color coded. B, Plot of saccade endpoint relative to the origin where the x- and y-axes represent horizontal and vertical components, respectively, and the time integral taken over the saccade interval of the corresponding LFP response is color coded. Note that, regardless of direction, as the amplitude of the saccades made become larger, the peak LFP becomes increasingly negative. Left and right insets show a constant LFP response as a function of saccade direction and a lack of unit activity during saccades (5 to 10 deg) made in the contralateral and ipsilateral direction, respectively.