Sensorimotor cortex injury effects on recovery of contralesional dexterous movements in Macaca mulatta

Abstract

The effects of primary somatosensory cortex (S1) injury on recovery of contralateral upper limb reaching and grasping was studied by comparing the consequences of isolated lesions to the arm/hand region of primary motor cortex (M1) and lateral premotor cortex (LPMC) to lesions of these same areas plus anterior parietal cortex (S1 and rostral area PE). We used multiple linear regression to assess the effects of gray and white matter lesion volumes on deficits in reaching and fine motor performance during the first month after the lesion, and during recovery of function over 3, 6 and 12 months post-injury in 13 monkeys. Subjects with frontoparietal lesions exhibited larger deficits and poorer recovery as predicted, including one subject with extensive peri-Rolandic injury developing learned nonuse after showing signs of recovery. Regression analyses showed that total white matter lesion volume was strongly associated with initial post-lesion deficits in motor performance and with recovery of skill in reaching and manipulation. Multiple regression analyses using percent damage to caudal M1 (M1c), rostral S1 (S1r), LPMC and area PE as predictor variables showed that S1r lesion volumes were closely related to delayed post-lesion recovery of upper limb function, as well as lower skill level of recovery. In contrast, M1c lesion volume was related primarily to initial post-lesion deficits in hand motor performance. Overall, these findings demonstrate that frontoparietal injury impairs hand motor function more so than frontal motor injury alone, and results in slower and poorer recovery than lesions limited to frontal motor cortex.

Terminal organization of the corticospinal projection from the lateral premotor cortex to the cervical enlargement (C5–T1) in rhesus monkey

“…This would indicate LPMCd CSP proliferation may occur in spinal subsectors mediating proximal limb recovery (e.g., bilaterally in medial lamina VII and lamina VIII). In this regard, a spared LPMCd CSP appears to be in a favorable position to contribute to recovery of postural stabilization and reaching, particularly following compromise of the shoulder/trunk representation of M1 which lies caudal to LPMCd, and directly dorsal to the M1 arm/hand area (Figure 17a, see area outlined by the dashed red line) (Boudrias et al, 2010;Darling et al, 2013Darling et al, , 2016Hudson, Park, Belhaj-Saif, & Cheney, 2017;Kwan, Mackay, Murphy, & Wong, 1978a,b;Weinrich & Wise, 1982).…”

Hand Motor Recovery Following Extensive Frontoparietal Cortical Injury Is Accompanied by Upregulated Corticoreticular Projections in Monkey

“…The mechanisms underlying recovery of upper-limb motor function after damage to the sensorimotor system due to stroke and traumatic brain injury are the focus of considerable research (Nudo, 2013;Baker et al, 2015;Carmichael et al, 2017;Ward, 2017). Because the motor system exhibits parallel distributed Figure 1.…”

“…Line drawings of the lateral surface of the injured hemisphere of four cases with F2 lesions (top) and five cases with F2P2 lesions (bottom). For detailed descriptions of the lesion sites, FD injection sites in spared iM2, and affiliated ICMS maps, see McNeal et al (2010) and Morecraft et al (2015aMorecraft et al ( , 2016. cs, Central sulcus; ilas, inferior limb of the arcuate sulcus; ios, inferior occipital sulcus; ipcd, inferior precentral dimple; ips, intraparietal sulcus; lf, lateral fissure; LPMCd, dorsolateral premotor cortex; LPMCv, ventrolateral premotor cortex; ls, lunate sulcus; M1r, rostral M1; PE, architectonic area of the superior parietal lobule (Pandya and Seltzer, 1982); ps, principle sulcus; S1c, caudal primary somatosensory cortex; SDM, South Dakota Monkey; slas, superior limb of the arcuate sulcus; sts, superior temporal sulcus.…”

“…Second, we recently observed that damage to the postcentral somatosensory cortex, in addition to precentral motor cortex injury (type-F2P2 lesion), results in deterioration of the intact iM2 CSP to C5-T1 but results in variable levels of recovery of fine motor function in the hand (Morecraft et al, 2015a). Such F2P2 lesions also blocked a favorable upregulated response in the contralesional M1 (cM1) CSP to ipsilateral C5-T1, preventing a CSP contribution to hand motor recovery from cM1 (Morecraft et al, 2016). Thus, macaque monkeys can apparently recover fine motor function, including precision grasp, after severe damage to the lateral sensorimotor cortex.…”

Assessment of the effect of continuous theta burst stimulation of the motor cortex on manual dexterity in non‐human primates in a direct comparison with invasive intracortical pharmacological inactivation

“…Manual dexterity in non‐human primates is an adequate behavioural readout to study the effects of a motor cortex lesion (Darling et al., ; Morecraft et al., ; Schmidlin et al., ; Wyss et al., ), as well as the subsequent functional recovery due to cortical plasticity. Indeed, fine motor control such as precision grip involved in manual dexterity is a characteristic of primates (Lawrence, Porter, & Redman, ; Lemon, ; Lemon & Griffiths, ; Rouse & Schieber, ).…”