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

Abstract

There are substantial differences across species in the organization and function of the motor pathways. These differences extend to basic electrophysiological properties. Thus, in rat motor cortex, pyramidal cells have long duration action potentials, while in the macaque, some pyramidal neurons exhibit short duration “thin” spikes. These differences may be related to the expression of the fast potassium channel Kv3.1b, which in rat interneurons is associated with generation of thin spikes. Rat pyramidal cells typically lack these channels, while there are reports that they are present in macaque pyramids. Here we made a systematic, quantitative comparison of the Kv3.1b expression in sections from macaque and rat motor cortex, using two different antibodies (NeuroMab, Millipore). As our standard reference, we examined, in the same sections, Kv3.1b staining in parvalbumin‐positive interneurons, which show strong Kv3.1b immunoreactivity. In macaque motor cortex, a large sample of pyramidal neurons were nearly all found to express Kv3.1b in their soma membranes. These labeled neurons were identified as pyramidal based either by expression of SMI32 (a pyramidal marker), or by their shape and size, and lack of expression of parvalbumin (a marker for some classes of interneuron). Large (Betz cells), medium, and small pyramidal neurons all expressed Kv3.1b. In rat motor cortex, SMI32‐postive pyramidal neurons expressing Kv3.1b were very rare and weakly stained. Thus, there is a marked species difference in the immunoreactivity of Kv3.1b in pyramidal neurons, and this may be one of the factors explaining the pronounced electrophysiological differences between rat and macaque pyramidal neurons.

Cortical states control visual spatial perception

“…However, decorrelation and FS neuron activity did not predict behavior better than RS firing rates, at odds with findings in primates (Mitchell et al, 2007;Snyder et al, 2016). This may be due to differences in RS and FS neuron identification in higher mammals (Constantinople et al, 2009;Soares et al, 2017;Vigneswaran et al, 2011). In mice, >90% of FS neurons are PV inhibitory neurons, and >90% of RS neurons are excitatory neurons (Lee et al, 2010;Pfeffer et al, 2013;Rudy et al, 2011), enabling clearer interpretation of roles of cell types.…”

“…Reduction of correlated activity (decorrelation) best accounts for perceptual improvements in these tasks (Cohen and Maunsell, 2009), but the neuronal subtypes involved remain unclear. Identifying cortical neuron subtypes in higher mammals presents challenges, since action potentials of many excitatory neurons are indistinguishable from those of inhibitory neurons (Constantinople et al, 2009;Haider et al, 2010;Soares et al, 2017;Vigneswaran et al, 2011). This may hinder full understanding of excitatory and inhibitory contributions to decorrelation and sensory perception.…”

Comparative morphology of gigantopyramidal neurons in primary motor cortex across mammals

“…Specific to the present study, the variable distribution exhibited by gigantopyramidal neurons within a single species (Rivara et al, ) is further compounded here by the inclusion of multiple species that have not yet been extensively studied for M1 somatotopic representation. The exact electrophysiological properties of neurons in M1 in general, and the hand‐forepaw region in particular, remain less clear across many of these species than for well‐researched laboratory animals (e.g., macaque; Soares et al, ). As such, the gigantopyramidal neurons in the present sample may not represent a homogenous, physiologically equivalent population, which induces additional variability.…”

“…They have also been shown in macaque monkeys to express parvalbumin‐like immunoreactivity (Preuss & Kaas, ) and have stained densely for cytochrome oxidase (Matelli, Luppino, & Rizzolatti, ), both of which indicate potentially high firing rates and metabolic activity. Finally, current evidence suggests that large layer V pyramidal neurons, including gigantopyramidal neurons, in macaque M1 express the fast potassium channel, Kv3.1b, which has been associated with high‐frequency, short duration action potentials typical of corticofugal pyramidal neurons (Ichinohe et al ; Soares et al, ).…”

Cortical influences drive amyotrophic lateral sclerosis

“…Corticospinal neurons in primates exhibit a number of key features which distinguish them from those in rodents, including short duration spikes,55 some fibres with fast conduction velocities54 and widespread expression of the fast K+ channel Kv3.1b 56. These primate-specific features may in some way be related to the particular vulnerability of these neurons to TDP-43 pathology in humans.…”