Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys

Qi, Hui‐Xin; Gharbawie, Omar A.; Wynne, Katherine W.; Kaas, Jon H.

doi:10.1016/j.bbr.2013.05.058

Cited by 47 publications

(59 citation statements)

References 60 publications

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“…1B, and Table S1) and extended lesions to the dorsal column (monkeys S and N, Fig. 1B) (31) and/or to the ventral part of the lateral funiculus (monkey S; the extent of lesion was 70.4%; Fig. 1B and Table S1).…”

Section: Confirmation Of Blockade Of Synaptic Transmission Through Pnsmentioning

confidence: 99%

Contribution of propriospinal neurons to recovery of hand dexterity after corticospinal tract lesions in monkeys

Tohyama

Kinoshita

Kobayashi

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The direct cortico-motoneuronal connection is believed to be essential for the control of dexterous hand movements, such as precision grip in primates. It was reported, however, that even after lesion of the corticospinal tract (CST) at the C4-C5 segment, precision grip largely recovered within 1-3 mo, suggesting that the recovery depends on transmission through intercalated neurons rostral to the lesion, such as the propriospinal neurons (PNs) in the midcervical segments. To obtain direct evidence for the contribution of PNs to recovery after CST lesion, we applied a pathway-selective and reversible blocking method using double viral vectors to the PNs in six monkeys after CST lesions at C4-C5. In four monkeys that showed nearly full or partial recovery, transient blockade of PN transmission after recovery caused partial impairment of precision grip. In the other two monkeys, CST lesions were made under continuous blockade of PN transmission that outlasted the entire period of postoperative observation (3-4.5 mo). In these monkeys, precision grip recovery was not achieved. These results provide evidence for causal contribution of the PNs to recovery of hand dexterity after CST lesions; PN transmission is necessary for promoting the initial stage recovery; however, their contribution is only partial once the recovery is achieved.spinal cord injury | plasticity | neural circuit | nonhuman primates | viral vector A s a potential treatment for brain and spinal cord injury, regeneration of the injured axons has been attempted in animal models, often using rodents with corticospinal tract (CST) lesions. Regeneration of the injured CST fibers was facilitated by treatments such as peripheral nerve graft (1), application of an antibody against neurite growth inhibitors IN-1 (2), combined application of the antibody and neurotrophic factor NT-3 (3), and transplantation of neural stem cells derived from induced pluripotent stem cells (4). A more recent study showed that regenerated CST axons increased the connection to the spinal motoneurons (MNs) after spinal cord injury in monkeys (5). However, in these studies, the causal contribution of such regenerated fibers to the functional recovery was not directly demonstrated. Therefore, recent debates address the question whether these therapies should target repairing the injured CST fibers and/or facilitating compensation by indirect cortico-motoneuronal (CM) connections via other descending motor pathways (6-9).Traditionally, the neural control of dexterous hand movements in higher primates has primarily been associated with development of the direct pathway from the motor cortex to MNs, known as the CM pathway (10-12). Lesion of the CST at the brainstem level in nonhuman primates caused near-permanent loss of dexterous hand movements (13). The authors also argued for partial compensation of grasping movements by the brainstemmediated descending pathways such as the rubrospinal tract (14). More recent studies on the neural basis of functional recovery following CST lesions ...

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Section: Confirmation Of Blockade Of Synaptic Transmission Through Pnsmentioning

confidence: 99%

Contribution of propriospinal neurons to recovery of hand dexterity after corticospinal tract lesions in monkeys

Tohyama

Kinoshita

Kobayashi

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Bashir et al, 2012;Freund et al, 2006Freund et al, , 2009Kaeser et al, 2010Kaeser et al, , 2011Kaeser et al, , 2013Kaeser et al, , 2014Liu and Rouiller, 1999;Schmidlin et al, 2004Schmidlin et al, , 2005Schmidlin et al, , 2011Wyss et al, 2013), derived from an early initial version (Brinkman and Kuypers, 1973;Brinkman, 1984); (ii) the modified Klu¨ver board task to assess various types of finger grip, ranging from power grip to precision grip (e.g. Nudo et al, 1992;Xerri et al, 1998;Murata et al, 2008;Milliken et al, 2013;Qi et al, 2013;Sugiyama et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Role of primary motor cortex in the control of manual dexterity assessed via sequential bilateral lesion in the adult macaque monkey: A case study

et al. 2017

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Abstract-From a case study, we describe the impact of unilateral lesion of the hand area in the primary motor cortex (M1) on manual dexterity and the role of the intact contralesional M1 in long-term functional recovery. An adult macaque monkey performed two manual dexterity tasks: (i) ''modified Brinkman board" task, assessed simple precision grip versus complex precision grip, the latter involved a hand postural adjustment; (ii) ''modified Klü ver board" task, assessed movements ranging from power grip to precision grip, pre-shaping and grasping. Two consecutive unilateral M1 lesions targeted the hand area of each hemisphere, the second lesion was performed after stable, though incomplete, functional recovery from the primary lesion. Following each lesion, the manual dexterity of the contralesional hand was affected in a comparable manner, effects being progressively more deleterious from power grip to simple and then complex precision grips. Both tasks yielded consistent data, namely that the secondary M1 lesion did not have a significant impact on the recovered performance from the primary M1 lesion, which took place 5 months earlier. In conclusion, the intact contralesional M1 did not play a major role in the long-term functional recovery from a primary M1 lesion targeted to the hand area. Ó

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“…Limited numbers of studies have focused on detailed armreaching movements in spinalized nonhuman primates [18,22] and rodents [14,23,24]. These studies recorded the two-dimensional (2D) position of the hand joints during food retrieval movement at less than 67 frames/s.…”

Section: Introductionmentioning

confidence: 99%

“…These studies recorded the two-dimensional (2D) position of the hand joints during food retrieval movement at less than 67 frames/s. Evaluation indices were then calculated using the data on the hand positions, such as the reaching time [18,22], average reaching speed [18,24], hand preshaping [23], reaching path distance [18], and an analog rating of movement components [14,24]. However, there are several limitations to this strategy.…”

Section: Introductionmentioning

confidence: 99%

“…The number of patients with SCI is estimated to total Preclinical feasibility studies on loss and recovery mechanisms for forelimb motor function have been performed with experimental cervical SCI in rodents [3,[5][6][7][11][12][13][14][15][16] and nonhuman primates [4,[8][9][10]17], and various methods have been established to evaluate impaired upper limb motor function. For example, single pellet reaching tasks evaluate upper limb motor function based on a number of pellets retrieved within a certain time or the retrieval success rate [4,5,7,[11][12][13][14][15][16][17][18]. With respect to several models of cervical SCI in nonhuman primates, bar grip force [8,19,20] and open field scoring [9,10] have been used to evaluate upper limb motor impairment.…”

Section: Introductionmentioning

confidence: 99%

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Three-dimensional motion analysis of arm-reaching movements in healthy and hemispinalized common marmosets

Takemi

Kondo

Yoshino-Saito

et al. 2014

Behavioural Brain Research

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Spinal cord injury (SCI) is a devastating neurological injury. At present, pharmacological, regenerative, and rehabilitative approaches are widely studied as therapeutic interventions for motor recovery after SCI. Preclinical research has been performed on model animals with experimental SCI, and those studies often evaluate hand and arm motor function using various indices, such as the success rate of the single pellet reaching test and the grip force. However, compensatory movement strategies, involuntary muscle contraction, and the subject's motivation could affect the scores, resulting in failure to assess direct recovery from impairment. Identifying appropriate assessments of motor impairment is thus important for understanding the mechanisms of motor recovery. In this study, we developed a motion capture system capable of reconstructing three-dimensional hand positions with millimeter and millisecond accuracy and evaluated hand kinematics during food retrieval movement in both healthy and hemispinalized common marmosets. As a result, the endpoint jerk, representing the accuracy of hand motor control, was asserted to be an appropriate index of upper limb motor impairment by eliminating the influence of the subject's motivation, involuntary muscle contraction, and compensatory strategies. The result also suggested that the kinematics of the limb more consistently reflects motor restoration from deficit due to spinal cord injury than the performance in the single pellet reaching test. Because of recent attention devoted to the common marmoset as a nonhuman primate model for human diseases, the present study, which clarified arm-reaching movements in spinalized marmosets, provides fundamental knowledge for future therapeutic studies.

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Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys

Cited by 47 publications

References 60 publications

Contribution of propriospinal neurons to recovery of hand dexterity after corticospinal tract lesions in monkeys

Contribution of propriospinal neurons to recovery of hand dexterity after corticospinal tract lesions in monkeys

Role of primary motor cortex in the control of manual dexterity assessed via sequential bilateral lesion in the adult macaque monkey: A case study

Three-dimensional motion analysis of arm-reaching movements in healthy and hemispinalized common marmosets

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