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Articles, Behavioral/Systems/Cognitive

Large Identified Pyramidal Cells in Macaque Motor and Premotor Cortex Exhibit “Thin Spikes”: Implications for Cell Type Classification

Ganesh Vigneswaran, Alexander Kraskov and Roger N. Lemon
Journal of Neuroscience 5 October 2011, 31 (40) 14235-14242; DOI: https://doi.org/10.1523/JNEUROSCI.3142-11.2011
Ganesh Vigneswaran
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Alexander Kraskov
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Roger N. Lemon
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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 (R2 = 0.40, p < 0.001) and F5 (R2 = 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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The Journal of Neuroscience: 31 (40)
Journal of Neuroscience
Vol. 31, Issue 40
5 Oct 2011
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Large Identified Pyramidal Cells in Macaque Motor and Premotor Cortex Exhibit “Thin Spikes”: Implications for Cell Type Classification
Ganesh Vigneswaran, Alexander Kraskov, Roger N. Lemon
Journal of Neuroscience 5 October 2011, 31 (40) 14235-14242; DOI: 10.1523/JNEUROSCI.3142-11.2011

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Large Identified Pyramidal Cells in Macaque Motor and Premotor Cortex Exhibit “Thin Spikes”: Implications for Cell Type Classification
Ganesh Vigneswaran, Alexander Kraskov, Roger N. Lemon
Journal of Neuroscience 5 October 2011, 31 (40) 14235-14242; DOI: 10.1523/JNEUROSCI.3142-11.2011
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  • Reforming our ideas about cell types and spike waveforms
    Lucas L. Sjulson
    Published on: 29 November 2011
  • Published on: (29 November 2011)
    Reforming our ideas about cell types and spike waveforms
    • Lucas L. Sjulson, Postdoctoral fellow
    • Other Contributors:
      • Jens Hjerling-Leffler, Bernardo Rudy, Gordon Fishell

    Since the pioneering work of Mountcastle, there has been great enthusiasm for the notion that single unit activity could be attributed to specific cell types based on extracellular spike waveforms. The current work by Lemon and Colleagues (Vigneswaran et al., 2011) highlights a previously unrecognized caveat of this approach by demonstrating that a subset of pyramidal cells have narrow spikes and could easily be misclas...

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    Since the pioneering work of Mountcastle, there has been great enthusiasm for the notion that single unit activity could be attributed to specific cell types based on extracellular spike waveforms. The current work by Lemon and Colleagues (Vigneswaran et al., 2011) highlights a previously unrecognized caveat of this approach by demonstrating that a subset of pyramidal cells have narrow spikes and could easily be misclassified as interneurons. Complicating matters further, we would point out an additional caveat, that a substantial proportion of interneurons have broad spikes and could conversely be misclassified as pyramidal cells. Recent results from our group obtained using unbiased techniques show that prior studies had underestimated the size of the interneuron population that is not fast-spiking, which we have found constitutes approximately 60% of the interneurons in mouse somatosensory cortex (Rudy et al., 2011). Intracellular recordings in awake behaving mice have demonstrated that some non-fast-spiking interneurons can not be distinguished from pyramidal cells based on spike waveform alone (Gentet et al., 2010), and although a similar in vivo study has not been performed in primates, intracellular slice recordings from primate cortex show similar broad spike waveforms for a large subset of interneurons (Zaitsev et al., 2009). Further complicating the picture, the proportion of GABAergic interneurons expressing narrow-spiking markers varies substantially between rodents and primates, as well as between different cortical areas (Constantinople et al., 2009). Hence as revealed by both the Vigneswaran et al. work and our own, unambiguous extracellular identification of neurons requires the use of other techniques, such as optogenetic stimulation (Lima et al., 2009). We therefore join the authors in encouraging the extracellular recording community to exercise caution when inferring cell type based on spike waveforms.

    References:

    Constantinople CM, Disney AA, Maffie J, Rudy B, Hawken MJ (2009) Quantitative analysis of neurons with Kv3 potassium channel subunits, Kv3.1b and Kv3.2, in macaque primary visual cortex. J Comp Neurol 516:291- 311.

    Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CC (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422-435.

    Lima SQ, Hromadka T, Znamenskiy P, Zador AM (2009) PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS One 4:e6099.

    Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45-61.

    Vigneswaran G, Kraskov A, Lemon RN (2011) Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 31:14235-14242.

    Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA (2009) Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cereb Cortex 19:1597-1615.

    Conflict of Interest:

    None declared

    Show Less
    Competing Interests: None declared.

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