Chapter 3. Spike-field coherence during performance monitoring and cognitive control
3.2 Results
3.2.1 Spike-field coherence signature of action outcome monitoring
To gain further insight into the mechanisms that generate the error signals encoded by error neurons, we analyzed local relationships between the LFP and spikes in MFC.
Neurons can organize dynamically into assemblies to increase the information saliency, in order to transmit information efficiently to downstream targets (Riehle et al., 1997, Wong et al., 2016, Salinas and Sejnowski, 2001). Given the saliency of errors, we reasoned that neurons in the MFC might form such dynamic assemblies to effectively represent and transmit error information. We measured the extent of each neuron's participation in such an assembly using spike-field coherence (SFC), which quantifies the precision of spike timing of a given neuron relative to the phase of ongoing oscillatory activity in the LFP (Fries et al., 2001, Wong et al., 2016, Rutishauser et al., 2010). The following analysis is based on LFP recorded on the same microwire as each neuron.
SFC between spikes of all recorded MFC neurons and the low frequency (< 4Hz) component of the LFP increased significantly following errors (Fig. 3.1a-c; p < 0.01 for all clusters; contours derived from the cluster-based permutation tests). This increase was accompanied by a simultaneous decrease in SFC to higher frequency 5-10 Hz LFP components (Fig. 3.1b,c; comparisons based on the ‘SFC modulation index’; see Eq. 1 in Methods; p < 0.01 for all clusters; contours derived from the cluster-based permutation tests). These patterns of changes in SFC were not seen during correct trials. The low- frequency error-related SFC modulation emerged first in pre-SMA (Fig. 3.1b,c), consistent with a leading role of this brain region. This modulation of SFC was prominent at both the single neuron level (Fig. 3.1a shows examples) as well as at the population level in both brain regions for all recorded neurons (Fig. 3.1b,c) and error neurons alone (Fig. 3.2).
Similar patterns of SFC modulation were also seen when considering error neurons alone (Fig. 3.2). In summary, neurons phase-locked to low frequency components of the LFP (<
4Hz) only after errors, suggesting a mechanism whereby error neuron responses are generated through transient functional ensembles that are formed depending on action outcomes.
Figure 3.1 Spike-field coherence during errors predicts engagement of control
(a) Spike-trigger average (STA) and spike-field coherence (SFC) for four example neurons (red for error, green for correct). Thin lines, raw STA; thick lines, STA filtered with 2-5Hz fourth-ordered Butterworth band-pass filter. Note the prominent 2-5Hz oscillations in the error STA (red) and that the SFC captures this feature.
(b) SFC modulation index (see Eq. 1 in methods) as a function of time and frequency averaged across all recorded dACC neurons (n= 256). Contour lines delineate significant clusters (p < 0.01) as determined by a cluster-based permutation test. During errors, there was an increase in SFC in the 2-5Hz frequency range with a simultaneous reduction in SFC in the higher (5-10Hz) frequency range. During correct trials, these same neurons increased SFC only in the higher 6-8Hz frequency band.
(c) Same as (b), but for pre-SMA neurons (n = 392). During errors, there was an increase in SFC in the 2- 4Hz frequency range with a simultaneous reduction in SFC in the higher (5-10Hz) frequency range. During correct trials, these same neurons increased SFC only in the higher 3-6Hz frequency band.
(d) Error signals alone did not predict the strength of PES. The PES modulation index is defined as the difference between errors that lead to more PES (upper 50% of PES) and those that lead to less PES (lower
50% of PES) divided by their sum (see Eq. 2 in methods). Here, the index was computed using iERN amplitude and spike rates of error neurons (Type I). All comparisons versus zero were not significant (p >
0.1; t-test).
(e) SFC predicts strength of behavioral control following errors as measured by post-error slowing (PES), for error neurons in pre-SMA. (left) Shown is the PES modulation index computed using SFC as a function of frequency (left; Type I and II error neurons pooled; 1 to 2s post-action). Grey shading delineates frequencies with a significant difference as determined by a cluster-based permutation test (p = 0.003). (right) Firing rates and power (as assessed by spike-triggered power, see methods) in the same time window and frequency range (1 to 2s post-action, 3-6 Hz, as determined from left side) did not predict the extent of PES (p > 0.1 for both comparisons, t-test versus 0). By contrast, the SFC was predictive (p < 0.001, t-test versus 0; see also left side).
‘*’, ‘**’, and ‘***’ mark statistical comparisons with p value ≤ 0.05, ≤ 0.01, or ≤ 0.001, respectively. Error bars represent ± s.e.m across cells. All data used in this figure were recorded using micro-electrodes.
3.2.2 Spike-field coherence during errors predicts the extent of post-error slowing
Given the strong error-related modulation of the SFC, we next investigated whether the SFC might serve as a mechanism for engaging behavioral control processes.
Specifically, we tested whether the strength of SFC on an error trial predicts the extent of slowing in the next trial (PES). We again partitioned error trials based on a median-split of the PES magnitude. We then compared whether neural signals differentiated between these two groups using the “more/less PES modulation index” (see Eq. 2 in Methods). We found that the error signals analyzed above (spike rates of error neurons in the 0-1s after the erroneous actions and iERN amplitude) did not predict the extent of post-error slowing (Fig. 3.2d; p > 0.1 for all comparisons versus zero using t-test). By contrast, the SFC was predictive: the strength of SFC computed using spikes emitted by pre-SMA error neurons during later part of error trials (1-2s after the erroneous actions) predicted the extent of reaction time slowing on the next trial (Fig. 3.2e; more vs. less PES, p = 0.003, significant frequency range was obtained by cluster-based permutation tests; significant after Bonferroni’s correction at the level of q = 0.0125). This effect was only significant for error neurons in pre-SMA (both Type I and Type II), but not for those in dACC or non-error neurons in either brain region (p > 0.05, cluster-based permutation tests). In addition, the SFC computed with spikes emitted by pre-SMA error neuron in the early part of error trials (0-1s after button press) was not predictive. This result suggests that engagement of behavioral control follows error detection. As a comparison, we also tested whether spike rates or LFP power in this later time window (thus the same data used to compute SFC that is predictive of PES) could also predict the extent of PES (see Methods for details). We found that these metrics were not predictive of PES (Fig. 3.2e, bar plots), highlighting the importance of spike timing of error neurons relative to ongoing oscillations in engaging behavioral control.
Figure 3.2 Spike-field coherence of error neurons
(a) SFC modulation index (see Eq 1 methods) as a function of time and frequency for error neurons in the dACC (Type I and type II pooled; n= 74). Contour lines delineate significant clusters (p < 0.05) as determined by a cluster-based permutation test. During errors (left), there was an increase in SFC in the 2-5Hz frequency range with a simultaneous reduction in SFC in the higher (5-10Hz) frequency range. This pattern was not seen during correct trials (right).
(c) Same as (b), but for pre-SMA error neurons (Type I and type II pooled; n = 163). Contour lines delineate significant clusters (p < 0.01) as determined by a cluster-based permutation test. During errors, there was an increase in SFC in the 2-4Hz frequency range with a simultaneous reduction in SFC in the higher (5-10Hz) frequency range. During correct trials, these same neurons increased SFC only to the higher 3-6Hz frequency band. This pattern is consistent with using all the neurons in pre-SMA (Fig. 5b, right).