Intracortical Microstimulation Maps of Motor, Somatosensory, and Posterior Parietal Cortex in Tree Shrews (Tupaia belangeri) Reveal Complex Movement Representations

Abstract

Long-train intracortical microstimulation (LT-ICMS) is a popular method for studying the organization of motor and posterior parietal cortex (PPC) in mammals. In primates, LT-ICMS evokes both multijoint and multiple-body-part movements in primary motor, premotor, and PPC. In rodents, LT-ICMS evokes complex movements of a single limb in motor cortex. Unfortunately, very little is known about motor/PPC organization in other mammals. Tree shrews are closely related to both primates and rodents and could provide insights into the evolution of complex movement domains in primates. The present study investigated the extent of cortex in which movements could be evoked with ICMS and the characteristics of movements elicited using both short train (ST) and LT-ICMS in tree shrews. We demonstrate that LT-ICMS and ST-ICMS maps are similar, with the movements elicited with ST-ICMS being truncated versions of those elicited with LT-ICMS. In addition, LT-ICMS-evoked complex movements within motor cortex similar to those in rodents. More complex movements involving multiple body parts such as the hand and mouth were also elicited in motor cortex and PPC, as in primates. Our results suggest that complex movement networks present in PPC and motor cortex were present in mammals prior to the emergence of primates.

Keywords: evolution; grasping; motor cortex; primate; reaching.

Figure 1.

Phylogenetic tree representing the relationship of mammals within the Euarchontoglires clade, which includes rodents, rabbits and pikas, tree shrews, and primates.

Figure 2.

Experimental set-up. Tree shrews were placed in individually designed hammocks such that all 4 limbs could move freely. Their heads were secured with a head post, and the electrode was lowered using a micromanipulator. The hammock, head post, and micromanipulator were all attached to the same stereotax.

Figure 3.

Alignment of motor maps with cortical architecture. Photographs taken during cortical mapping ( A ) were aligned to architectonic sections by matching the surface blood vasculature patterns in the photos with the most superficial tissue sections stained for CO ( B ) to reveal surface blood vessel patterns. A prominent star-shaped vascular pattern in ( B ) is highlighted in ( A ) (additionally, during mapping, fluorescent fiducial probes were placed in various locations to aid in our alignment of ICMS maps to histologically processed tissue). Common blood vessel patterns (black and white arrowheads in ( B , C ) were used to align deeper tissue sections that revealed areal borders.

Figure 4.

Example of fluorescent fiduciary probes used to help align motor maps with cortical architecture. In this example, fiduciary probes were placed at the end of motor mapping using the anatomical fluorescent tracer, fluoro ruby (FR: 15% in phosphate buffered saline: Thermo Fisher Scientific). ( A ) Photograph of a myelin section under fluorescent light showing the location of the FR probes (2 white sites within photograph), with the architectonic borders superimposed over the photograph (gray lines). ( B ) Photograph of the same myelin section under brightfield highlighting the myeloarchitecture used to determine cortical borders (white and black lines).

Figure 5.

Myeloarchitecture of the tree shrew cortex from a single section of flattened cortical tissue. Areal borders for areas 17/V1, 3b, and auditory cortex are easily identified as darkly staining regions of cortex. Scale bar is 2 mm.

Figure 6.

Short-train (ST, 50 ms) and long-train (LT, 500 ms) intracortical microstimulation (ICMS) maps of Case 14–88. ( A ) Entire flattened cortical hemisphere with anatomical borders indicated with solid black lines. The gray region represents tissue that was located along the medial wall prior to flattening. The boxed region is enlarged in Panels ( C , D ) and ( E ). ( B ) Color-coded legend of joints and body parts moving during ICMS and the corresponding location on the lateral view of the tree shrew body. This legend is used for Figures  6 , 7 , 11 , and 12 . Different colors are used to indicate the types of movements elicited at different locations within panels ( C ) and ( D ). ( C ) ST-ICMS motor map. White dots represent the location of penetration sites where ICMS-evoked movements. Surrounding color tiles represent the location of the body moving during ST-ICMS. Striped tiles indicate multiple simultaneous movements. Solid black lines represent borders of cortical areas based on myelin. ( D ) LT-ICMS motor map. ( E ) Map of ratios in stimulation current thresholds required to elicit motor movements. Darker orange and red colored tiles indicate greater ratios of ST:LT thresholds. Burgundy tiles indicate no ST-evoked movements up to 500 μA, and white tiles indicate sites where threshold values were not measured. For the most part, greater currents were required to elicit movements using ST- versus LT-ICMS (at one site, shown in green, LT threshold > ST threshold).

Figure 7.

Short-train (ST, 50 ms) and long-train (LT, 500 ms) intracortical microstimulation (ICMS) maps of Case 14–89. ( A ) Flattened cortical hemisphere with anatomical borders indicated. ( B ) ST-ICMS motor map. ( C ) LT ICMS motor map. ( D ) and ( E ) Map of ratios in stimulation current thresholds required to elicit motor movements. Greater currents were required to elicit movements using ST- versus LT-ICMS ( D ); however, most thresholds are similar for 500 and 800 ms trains, that is, threshold _{500 ms} : threshold _{800 ms} ratio was near 1 ( E ). See Figure  6 for figure conventions.

Figure 8.

Example of ICMS-elicited movements using short-train (ST: 50 ms), long-train (LT: 500 ms), and extra-long-train (xLT: 800 ms) stimulation parameters. The black traces represent the baseline position of the forelimb. The trace with the darkest shade of gray represents the position of the hand 48 ms after stimulus onset, while progressively lighter shades of gray traces indicate progressively later positions of the arm and hand subsequent time points up to 800 ms. The black star represents the point on the hand used to measure the forelimb displacement, which is plotted below each movement example. The gray shading within the plot represents the period of time stimulation was presented.

Figure 9.

Example of an ICMS-elicited repeated movement using 3 different stimulation train durations at a single penetration site within area 3a of case 14–88 (Fig.  6 ). The top panel shows the lateral view of the tree shrew face at different points in time during stimulation. Stimulation caused the jaw to move downward and then upward. This motion was repeated multiple times with increased stimulation duration (50 ms left, 500 ms center, and 800 ms right). Black tracings represent the resting state position of the jaw prior to stimulation, dark gray, the position of the jaw at the maximum extent of the first downward movement in the movement series. The black star represents the point on the jaw used to measure the displacement plotted at bottom. The gray shading within the plot represents the period of time stimulation was presented.

Figure 10.

Examples of a simple and complex movements evoked from various cortical fields using long-train intracortical microstimulation. ( A ) An example of a simple movement involving the forelimb evoked during stimulation to a site within the posterior parietal cortex. The black trace represents the location of the forelimb prior to stimulation; the gray trace represents the location of the arm at the apex of the movement. ( B ) An example of complex movement involving both ipsilateral (ipsi-black and gray dashed line traces) and contralateral (contra—black and gray solid line traces) forelimbs and the contralateral hindlimb. ( C ) Movement evoked by LT-ICMS in motor cortex. Both hands move upward toward the mouth with elbow flexion, while the jaw opens. ( D ) Elbow flexion with eye squint evoked by LT-ICMS in Sc.

Figure 11.

LT-ICMS maps of Case 14–39 ( A ) and Case 14–124 ( B ) with corresponding threshold maps in which larger black circles indicate sites where movements could be evoked with smaller currents (14–39: C ), (14–124: D ). Other conventions as in previous figures.

Figure 12.

LT-ICMS maps for Cases 14–36 ( A ) and 14–93 ( B ) with corresponding threshold maps (14–36: C ), (14–93: D ). Other figure conventions are the same as those described in previous figures.

Figure 13.

Comparisons of motor maps across different mammals within the Euarchontoglires clade including rats ( A , B ), tree shrews ( C , D ), and prosimian galagos ( E , F ). General color-coded motor maps across all cortical areas are presented on the left column ( A , C , E ), while the location of possible movement domains within cortical areas is presented to the right ( B , D , F ). ( C , D ), The current results, with the location of possible movement domains within motor, posterior parietal cortex, as well as primary somatosensory cortex (3b). The rat map is based on results from Brecht et al. 2004 ; Tandon et al. 2008 ; and Brown and Teskey 2014 . Movements involving the eyes are located along the medial wall ( Brecht et al. 2004 ). Prosimian primate movement domains have been reported in motor, premotor, and posterior parietal cortex by Stepniewska et al. 2005 , , .