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Comparative Study
. 2011 Oct 5;31(40):14235-42.
doi: 10.1523/JNEUROSCI.3142-11.2011.

Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification

Ganesh Vigneswaran  1 , Alexander Kraskov, Roger N Lemon
Affiliations
Comparative Study

Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification

Ganesh Vigneswaran et al. J Neurosci. .

Abstract

Recent studies have suggested that extracellular recordings of putative cortical interneurons have briefer spikes than those of pyramidal neurons, providing a means of identifying cortical cell types in recordings from awake monkeys. To test this, we investigated the spike duration of antidromically identified pyramidal tract neurons (PTNs) recorded from primary motor (M1) or ventral premotor cortex (area F5) in 4 awake macaque monkeys. M1 antidromic latencies (ADLs) were skewed toward short ADLs (151 PTNs; 0.5-5.5 ms, median 1.1 ms) and significantly different from that of F5 ADLs (54 PTNs; 1.0-6.9 ms, median 2.6 ms). The duration of PTN spikes, recorded with a high-pass filter of 300 Hz and measured from the negative trough to the positive peak of the spike waveform, ranged from 0.15 to 0.71 ms. Importantly, we found a positive linear correlation between ADL and spike duration in both M1 (R(2) = 0.40, p < 0.001) and F5 (R(2) = 0.57, p < 0.001). Thus PTNs with the shortest ADL (fastest axons) had the briefest spikes, and since PTN soma size is correlated with axon size and conduction velocity, it is likely that the largest pyramidal neurons (Betz cells in M1) have spikes with short durations (0.15-0.45 ms), which overlap heavily with those reported for putative interneurons in previous studies in non-primates. In summary, one class of physiologically identified cortical pyramidal neuron exhibits a wide variety of spike durations and the results suggest that spike duration alone may not be a reliable indicator of cell type.

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Figures

Figure 1.
Figure 1.
Probability density functions comparing antidromic latencies of identified PTNs. Distributions are shown for M1 (blue) and F5 (green) PTNs. Binwidth 0.25 ms. The two vertical lines correspond to the median antidromic latency for each population of PTNs (1.1 and 2.6 ms for M1 and F5, respectively). The two median values are significantly different (p < 0.0001, Wilcoxon rank-sum test). Inset shows the antidromic response of an M1 PTN (heavy trace, average of 40 sweeps). Arrows indicate the onset of the PT stimulus and the onset of the antidromic spike. The antidromic latency of this PTN was 0.9 ms, spike duration was 0.24 ms. The thin trace shows collision of the antidromic spike by a spontaneous spike from this PTN, which occurred just before the PT stimulus.
Figure 2.
Figure 2.
Comparison of spike duration for recordings in filtered versus unfiltered conditions. The data points (light blue circles) have been approximated with a second-order polynomial (R2 = 0.99, light blue curve). Open circles correspond to UIDs and filled ones to PTNs. For filtered recordings we used a second-order causal high-pass Butterworth filter with a cutoff frequency of 300 Hz (the same filter as used in all the recordings reported here). Thick black line is the line of unity. The two insets show samples of unfiltered spike waveforms (black traces) from two PTNs, one with a narrow spike duration (0.22 ms) and one with a relatively wide spike (0.64 ms) and their filtered versions (light blue traces). All waveforms are averages of 1000 spikes. The duration of the filtered narrow spike decreased by 0.02 ms (11% reduction) whereas the filtered wide spike was reduced by 0.16 ms (26% reduction).
Figure 3.
Figure 3.
Spike durations of PTNs in M1 and F5. A, Probability density function of spike durations of identified PTNs in M1 (blue). Binwidth 0.025 ms. Vertical line corresponds to the median spike duration (0.26 ms). B, Probability density function of spike durations of identified PTNs in F5 (green). The median spike duration of M1 PTNs (0.26 ms) was significantly shorter than that for PTNs in F5 (0.43 ms) (p < 0.001, Wilcoxon rank-sum test). Inset shows splined averaged waveforms for two PTNs from M1 (blue, n = 32,943 spikes) and F5 (green, n = 1070). These waveforms have spike durations closest to the medians of their respective populations indicated in the main figure.
Figure 4.
Figure 4.
Spike durations of PTNs and unidentified neurons. A, Probability density function comparing spike durations of identified PTNs in M1 (blue) and M1 UIDs (yellow). Binwidth 0.025 ms. The two vertical lines correspond to the median spike duration for each population. The median spike duration of PTNs in M1 (0.26 ms) was not significantly different from that of UIDs in the same area (0.27 ms) (p > 0.8, Wilcoxon rank-sum test). Note that the UID population appears bimodal with a trough in the distribution at ∼0.4 ms and there is extensive overlap between the pyramidal and UID populations. B, Probability density function comparing spike durations of identified PTNs in F5 (green) and F5 UIDs (yellow). The two vertical lines correspond to the median spike duration for each population. The median spike duration of PTNs in F5 (0.43 ms) was again not significantly different from that of UIDs in the same area (0.35 ms) (p > 0.2, Wilcoxon rank-sum test). Note that there is considerable overlap between the two populations.
Figure 5.
Figure 5.
Positive correlation between PTN axon conduction velocity and spike duration. Scatter plot showing the positive correlation between antidromic latency (a surrogate for axonal conduction velocity and cell size) and spike duration for identified PTNs in areas M1 (blue) and F5 (green). The data have been fitted with a linear regression line shown in red. The correlation was highly significant (R2 = 0.51, p < 0.001). The light gray box indicates the range of spike durations (0.2–0.4 ms) that have been cited in the literature as a means of discriminating interneurons from pyramidal cells on the basis of spike duration (Table 2; see Discussion).
Figure 6.
Figure 6.
Relationship between peak-to-trough and peak-to-peak measures of spike duration. Scatter plot showing the relationship between spike duration as measured from the first negative trough to the subsequent peak of the extracellular waveform (trough-to-peak, as used in previous figures) and as measured from the first positive peak to the subsequent peak (peak-to-peak measure). Data from all identified PTNs in areas M1 and F5 (filled black circles). There was a significant correlation between the two measures of spike duration (R2 = 0.80, p < 0.0001). Note that the slope of the regression line (1.2, shown in red) and the intercept (106 μs) can be used to compare our measure of spike duration with others given in the literature (Table 2).
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