Of mice and monkeys: Somatosensory processing in two prominent animal models

Abstract

Our understanding of the neural basis of somatosensation is based largely on studies of the whisker system of mice and rats and the hands of macaque monkeys. Results across these animal models are often interpreted as providing direct insight into human somatosensation. Work on these systems has proceeded in parallel, capitalizing on the strengths of each model, but has rarely been considered as a whole. This lack of integration promotes a piecemeal understanding of somatosensation. Here, we examine the functions and morphologies of whiskers of mice and rats, the hands of macaque monkeys, and the somatosensory neuraxes of these three species. We then discuss how somatosensory information is encoded in their respective nervous systems, highlighting similarities and differences. We reflect on the limitations of these models of human somatosensation and consider key gaps in our understanding of the neural basis of somatosensation.

Keywords: Comparative neuroscience; Neural coding; Primates; Proprioception; Rats; Touch.

Figure 1.

A cladogram showing the phylogenetic relationship of five different mammals with each branching point indicating the time of the last common ancestor. Brains are drawn to (relative) scale except the human brain, which is substantially scaled down. The location of the primary somatosensory area, S1 (green), the primary visual area, V1 (yellow), and the posterior parietal cortex (PPC; blue) are depicted. Note that the relative size of the PPC is greatly expanded in primates, particularly in humans. From Goldring and Krubitzer, 2017.

Figure 2.. Functions of hands and whiskers.

Both whiskers and hands can sense object properties such as texture and shape, but only hands can grasp and manipulate objects.

Figure 3.. Innervation of the whisker follicle and fingertip.

A| Whisker follicles in mice and rats are complex encapsulated structures containing ~8 different mechanoreceptor types^,, including Merkel cell (cyan) and lanceolate-type (purple) endings. The responses of many types to sensory input remain unknown. The entire follicle rotates together with the whisker during whisking, due to the action of intrinsic and extrinsic muscles. B| The primate fingertip contains three main types of mechanoreceptors including Merkel cell (cyan), innervated by slowly adapting type 1 nerve fibers, Meissner corpuscles (red), innervated by rapidly adapting fibers, Pacinian corpuscles (blue), innervated by Pacinian corpuscle associated fibers. A fourth type, Ruffini endings (purple), innervated by slowly adapting type 2 fibers, is absent in macaques and sparse in human glabrous skin.

Figure 4.. The organization of somatosensory cortex in mice, rats and, macaque monkeys.

All three species have a primary somatosensory area (red), a second somatosensory area, and a parietal ventral area (pink). In macaque monkeys, additional areas that process somatosensory inputs have emerged over the course of evolution (green). Posterior parietal cortex has greatly expanded and includes multiple cortical fields in macaque monkeys. When mice and rat cortices are drawn to scale (D) the enormous difference in the size of the cortical sheet in these rodent models and macaque monkeys is striking. Adapted from Dooley and Krubitzer, 2013.

Figure 5.. Temporal precision and repeatability are hallmarks of both whisker and fingertip mechanoreceptors.

A| Responses evoked in primary afferents by repeated presentations of the same mechanical noise stimulus delivered to a whisker. The response is temporally patterned and highly repeatable. The same phenomenon is observed when analogous stimuli are delivered to the skin of macaque monkeys. Reproduced from Jones et al., 2004. B| Responses of a PC fiber to repeated presentations of a finely textured fabric. Left: Laser microscope image of the texture. Middle: Spiking response over 40 repeated presentations Right: Power spectra of the neuronal responses. When textures are scanned across the skin, PC fibers produce texture-specific temporal spiking patterns. Modified from Weber et al. (2013).

Figure 6.. Spatial coding by fingertip mechanoreceptors.

Spatial pattern of activation evoked in populations of SA1 (top row), RA (middle row), and PC fibers when embossed letters are scanned across the fingertip of macaques. The spatial layout of the stimulus is reflected in the spatial layout of the response it evokes in SA1 and RA fibers. Modified from Phillips et al., 1988.

Figure 7.. Direction tuning in area 1.

This neuron responds most strongly to an edge scanned across the skin in the distal to proximal direction and does not respond at all to the same edge scanned in the opposite direction. From Pei et al., 2010

Figure 8.. Forces and moments can be estimated during active touch in the whisker system.

A | Example frame (yellow box) from high-speed video of a mouse whisking with a single whisker against an object (indicated by overlaid red circle). The whisker follicle is denoted by the pink oval. Whisking against the object produces a whisker-object contact force, $\overrightarrow{F}$. B | Schematic showing the forces and bending moment that act in the plane of whisking. A whisker-object contact reaction force, $\overrightarrow{F}$, can be split into a lateral force $\left({\overrightarrow{F}}_{lat}\right)$ and an axial force $\left({\overrightarrow{F}}_{ax}\right)$ acting at the follicle, and produces a bending moment at the follicle $\left({\overrightarrow{M}}_0\right)$. These quantities can be estimated based on measurements obtained from high-speed video, together with measurements of whisker geometry. Modified from Pammer et al., 2013.

Figure 9.. Object localization during active touch.

Rats and mice scan their whiskers across regions near the face to localize objects in the azimuthal plane. The location of an object (black circle) within the region covered by a whisk cycle (pink-to-green gradient) can be determined by combining neural signals for whisker self-motion and whisker-object contact. These signals are encoded throughout the ascending somatosensory system (dashed lines). Modified from Mehta et al., 2007.