Expression of Kv3.1b potassium channel is widespread in macaque motor cortex pyramidal cells: A histological comparison between rat and macaque

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The descending motor pathways in mammals exhibit many species‐specific differences in both their structure and their function. Descending pathways originating from the cortex arise from layer V pyramidal neurons, and include corticostriatal, corticobulbar, corticopontine, and corticospinal projections, among others. For instance, species differences in the corticospinal system include variation in the cortical areas giving rise to the tract, in the size and distribution of corticospinal neurons and their axons, in the route these axons take within the spinal cord, and in their targets within the spinal gray matter (Kuypers, 1981; Lemon, 2008; Lemon & Griffiths, 2005). Differences in the organization of motor pathways are likely to reflect the variety of different functions that they mediate in different species.
In the rat, pyramidal neurons typically have action potentials with a broad duration (typically ∼900 µs), in contrast to many fast‐spiking cortical interneurons which exhibit much shorter duration spikes (∼400 µs; Bartho et al., 2004). Differences in spike duration between interneurons and pyramidal cells in rats are partly due to different levels of expression of Na+ and K+ channels (Bean, 2007; Erisir, Lau, Rudy, & Leonard, 1999; Martina & Jonas, 1997; Martina, Schultz, Ehmke, Monyer, & Jonas, 1998; Suter, Migliore, & Shepherd, 2013). Fast‐spiking properties reflect the presence of Kv3 and Kv1 channels which allow rapid repolarization. Kv3.1b mRNA and protein are associated with fast‐spiking interneurons in rats, which express parvalbumin (Bean, 2007; Rudy & McBain, 2001). The expression of Kv3.1b in rat pyramidal neurons is generally very low (Chow et al., 1999).
In contrast to the rat, in both the cat and macaque, pyramidal neurons can exhibit action potentials of short duration (Chen, Zhang, Hu, & Wu, 1996; Lemon, Vigneswaran, Waldert, Philipp, & Kraskov, 2012; Matsumura, 1979; Takahashi, 1965). In the awake macaque, extracellular recordings in primary motor cortex from identified corticospinal neurons (which are just one subclass of pyramidal neuron), have spikes as brief as 160 µs, with a mean duration of only 260 µs (Vigneswaran, Kraskov, & Lemon, 2011). The rapid repolarization of pyramidal neurons in the macaque could, in theory, allow very high spike discharge rates.
In keeping with this finding of brief spikes in macaque pyramidal neurons, there have been several reports of Kv3.1b being expressed in layer V pyramids in macaque cortex, including large pyramids in motor cortex (Constantinople, Disney, Maffie, Rudy, & Hawken, 2009; Ichinohe et al., 2004). However, there has never been a systematic comparison of Kv3.1b expression in rat and macaque motor cortex to reveal the extent to which pyramidal cells in monkey motor cortex express Kv3.1b potassium channels, and whether the expression of these channels is markedly different from that described in the rat.
In this study, we have used two different antibodies for Kv3.1b to make a direct comparison of its expression in rat and macaque cortical neurons, using parvalbumin‐expressing interneurons as a control cell population in both species. Pyramidal neurons were identified both by their characteristic shape and by labeling with the pyramidal cell neurofilament marker SMI32. This antibody has been described to label a large proportion of layer 3 and layer 5 pyramidal cells in the cortex of several species, including rat, monkey, and human (Campbell & Morrison, 1989; Gabernet, Meskenaite, & Hepp‐Reymond, 1999; Sternberger & Sternberger, 1983; Wakabayashi, Hansen, & Masliah, 1995). We measured the intensity of Kv3.1b expression in the soma membrane of these pyramidal neurons. We confirmed that in the rat motor cortex, very few SMI32‐postive pyramidal neurons express Kv3.1b, while its expression is common among macaque motor cortex pyramidal neurons. Labeled pyramids included large (Betz) cells, but also many smaller pyramidal neurons.
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