Cell and neuron densities in the primary motor cortex of primates

Abstract

Cell and neuron densities vary across the cortical sheet in a predictable manner across different primate species (Collins et al., 2010b). Primary motor cortex, M1, is characterized by lower neuron densities relative to other cortical areas. M1 contains a motor representation map of contralateral body parts from tail to tongue in a mediolateral sequence. Different functional movement representations within M1 likely require specialized microcircuitry for control of different body parts, and these differences in circuitry may be reflected by variation in cell and neuron densities. Here we determined cell and neuron densities for multiple sub-regions of M1 in six primate species, using the semi-automated flow fractionator method. The results verify previous reports of lower overall neuron densities in M1 compared to other parts of cortex in the six primate species examined. The most lateral regions of M1 that correspond to face and hand movement representations, are more neuron dense relative to medial locations in M1, which suggests differences in cortical circuitry within movement zones.

Keywords: M1; flow fractionator; isotropic fractionator; movement.

Figure 1

The location of the primary motor cortex (M1) on the lateral view of the left cerebral hemisphere in several of the primate species discussed in this paper. The location and internal organization of M1 in New world and Old World monkeys (Gould et al., ; Huang et al., ; Waters et al., ; Huntley and Jones, ; Donoghue et al., ; Nudo et al., ; Kaas, 2012) and prosimian galagos (Wu et al., 2000) consists of a fractured mosaic of smaller areas devoted to particular movements that are dispersed within a larger somatotopic framework of functional movement domains (see Kaas, ; Kaas et al., for review). Figure 1 shows the locations of M1 in prosimian galagos (Wu et al., ; Wong and Kaas, 2010), New World owl monkeys (Gould et al., 1986) and squirrel monkeys (Donoghue et al., ; Nudo et al., 1992), Old World macaques (Huntley and Jones, ; Preuss et al., 1997) and baboons (Waters et al., 1990), and Great Ape chimpanzees (Bailey et al., 1950). Hindlimb movement representations (foot) are located at the most dorsal-medial aspect of M1, and transitions to movements of the trunk of the body (trunk), forelimb and hand (hand), and finally face at the most ventral-lateral aspect of M1. Cortical areas located rostral to M1 include the dorsal (PMd) and ventral (PMv) premotor areas, the supplementary motor area (SMA), and frontal eye fields (FEF). Somatosensory areas of the anterior parietal cortex (3a, 3b, 1, 2) are caudal to M1. The location of the central sulcus (CS) is indicated in macaque, baboon, and chimpanzee.

Figure 2

The right cortical hemisphere of a galago (galago 3) was exposed, and movements were evoked at cortical sites in M1 with 60-ms microstimulation trains delivered to layer 5 (A). The locations of stimulation sites where movements were elicited are indicated by color-coded dots on the cortical surface. Somatosensory mapping of receptive fields (layer 4) responsive to tactile stimulation are indicated by color-coded squares on the cortical surface. Somatosensory mapping was undertaken to better identify the caudal boundary of M1. Boundaries of M1 and S1, and identifiable movement representations areas within M1, were marked with a fluororuby tracer (FR) immediately before sacrifice to estimate their location on the cortical surface (green stars). Following sacrifice, the brain was removed and the right cortical hemisphere was manually flattened (B). The FR-indicated areas were used as guidelines to conservatively dissect microstimulation-derived M1representations from remaining cortex. Dashed lines indicate dissections lines that resulted in 84 pieces for the entire cortical hemisphere. The dissection resulted in four pieces identified as M1 by microstimulation mapping (C). Areas dedicated to movements of the trunk, forelimb, and face were readily identified and efforts were made to dissect along these movement representations boundaries within M1. Each M1 piece, as well as cortical pieces medial and lateral to M1, had cell and neuron densities estimated using the flow fractionator method (D). The most lateral aspect of M1, which includes facial movement representations, is the most neuron dense area.

Figure 3

Histograms of cell and neuron density in M1 of Old World monkeys. Movement representation boundaries within M1 were estimated, the motor cortex was dissected along those boundaries, and cell and neuron densities were obtained using the flow fractionator. The results show that distribution of cells by mass (A) and by surface area (B) does not vary substantially within M1 in either the macaque (macaque 1; macaque 2) or baboon (baboon 1; baboon 2). Neuron density by mass (C) and surface area (D) shows a trend toward the most lateral aspect within M1, which includes face and hand movement representations, as being the most neuron dense area in both species. Please note that macaque 2 was an intact dissection and, as a result, cortical surface area could not be accurately estimated.