Elsevier

Behavioural Brain Research

Volume 252, 1 September 2013, Pages 363-376
Behavioural Brain Research

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

https://doi.org/10.1016/j.bbr.2013.05.058Get rights and content

Highlights

  • Hand use in a grasp task was evaluated pre- and post-dorsal column lesion in monkeys.

  • Damage to the sensory afferents at the cervical spinal cord produced impairment.

  • Spontaneous recovery was observed over weeks of testing.

  • The degree of behavioral recovery depended on the spared axons in the brainstem.

Abstract

Damage to the ascending forelimb afferents in the dorsal columns (DCs) of the cervical spinal cord in monkeys impairs forelimb use, particularly hand dexterity. Although considerable recovery has been reported, interpretation of the results is complicated by the reproducibility of the lesion and behavioral assessment. Here, we examined the effects of a unilateral DC lesion at the C4–C6 spinal cord level in four adult squirrel monkeys. Behavioral performance was assessed on a reach-to-grasp task over 5–13 weeks after lesion. Retrograde tracers were injected into the skin of the fingertips to determine the distribution of axon terminals in the cuneate nucleus and estimate the effectiveness of lesion at the conclusion of each case. The size and level of DC lesion was reflected in the proportion of spared afferents, which ranged from 1 to 25% across monkeys. The experiments produced two major findings. First, the extent of deafferentation in the DC is directly related to the degree of reaching and grasping impairments, and to the reactivation profile and somatotopic reorganization in contralateral primary somatosensory cortex. Second, considerable behavioral recovery and cortical reorganization occurred even in the monkey with only 1% of axons spared in the DC. Our findings suggest that cutaneous inputs from the hand and forelimb are critical to the integrity of functions such as reaching and grasping. In addition, axon branches from peripheral afferents that terminate on neurons in the dorsal horn of the spinal cord are likely central to the functional recovery.

Introduction

In primates, identifying surfaces and objects by manual touch is dependent on a multisynaptic pathway that connects cutaneous receptors in the hand with somatosensory cortex (see [1] for review). The first segment of this pathway is comprised of afferents that originate from slowly and rapidly adapting receptors on the glabrous and hairy surfaces of the hand. These afferents bifurcate as they enter the spinal cord. One branch of afferents terminates on neurons in the dorsal horn of the spinal cord. The other branch of afferents ascends in the DCs of the spinal cord and terminates in the cuneate nucleus. Damage to this segment of the pathway, such as from spinal cord injury, produces a range of behavioral impairments that include hand use. Understanding the contributions of somatosensory deafferentation to the behavioral deficits is complicated because of the non-selective nature of spinal cord injuries, which can damage descending fibers from the motor system. This confound can be overcome in animal models, particularly non-human primates, as the ascending sensory afferents are spatially segregated in the spinal cord from the descending motor projections.

Nevertheless, the extent of behavioral impairments reported in monkeys from interrupting sensory afferents varies considerably. For example, DC lesions in macaque monkeys have been reported to produce permanent deficits in precision grip and other digit movements [2], [3], [4], [5]. In contrast, other work showed that damage to the DC alone did not affect actions unless the dorsal lateral funiculus [6], [7], [8], [9], [10], or somatosensory cortex, is concurrently damaged [11]. Only one study examined the effects of DC section on actions in New World monkeys. Although the DC lesion did not affect reaching to grasp stationary targets, performance was impaired on an active bait catching task [12].

The size of the DC lesion and its rostrocaudal location along the spinal cord are predictive of afferent sparing and ultimately behavioral outcome. This assertion is perhaps best exemplified with an alternative experimental approach in which the afferents are severed at the dorsal roots, before entering into the spinal cord. For example, Mott and Sherrington [13] comprehensively severed the dorsal roots of the forelimbs of macaque monkeys, which completely abolished grasping. Darian-Smith and Ciferri [14] confirmed those findings with comprehensive deafferentation that was confined to the thumb and/or index fingers. Recovery was minimal or absent for at least 8 months of testing [14]. Nevertheless, incomplete deafferentation of the same dorsal roots also produced severe impairments at the outset, but substantial recovery of precision grip occurred in the postoperative weeks. Similarly, Mott and Sherrington [13] showed that sparing of a single dorsal root, irrespective of its origins from within the hand, produced milder deficits.

Determining the relationship between amount of deafferentation, degree of behavioral impairment, and time course of recovery, could improve our understanding of the consequences of DC lesions. We adapted the systematic approach developed for assessing reaching and grasping abilities in rats [15], [16] to measure the same abilities in squirrel monkeys. Addressing the following questions was our primary objective. (1) Does deafferentation from DC lesion affect dexterity during grasping? (2) Does deafferentation from DC lesion affect the forelimb trajectory during reaching? (3) What is the relationship between the extent of DC lesion and the severity of reaching and/or grasping impairments? (4) What is the time course of behavioral recovery? Some of the results have been previously presented in abstract form.

Section snippets

Material and methods

Four adult male squirrel monkeys (1 Saimiri sciureus and 3 Saimiri bolivians) were used for this study. Animals were 3–5 years old and weighed 800–1200 g. All experimental procedures were approved by the Vanderbilt University Animal Care and Use Committee, and followed the guideline of the National Institute of Health Guides for the Care and Use of Laboratory Animals.

Results

The goal of this study was to investigate the effects of DC section on reaching and grasping. Results are presented in three sections: First, extent of lesions; second, effects of lesions on performance in a reach-to-grasp task; and third, correlation between the amount of spared axon terminals in cuneate nucleus and performance in a reach-to-grasp task. As the extents and levels of the lesions varied, the results are presented on a case-by-case basis starting with the most impaired monkey.

Discussion

The main finding of the present study is that damage to the DC of the mid-cervical spinal cord affects reaching and grasping in squirrel monkeys. The degree of impairment and the potential for recovery is directly related to the amount of axon terminals spared in the cuneate nucleus. Nevertheless, the capacity for recovery should be interpreted cautiously because qualitative examination of the behavior after presumptive recovery shows that monkeys adopt alternate strategies to achieve the same

Conclusion

Our study shows that DC section impairs reaching and grasping in squirrel monkeys. The severity of the impairment and the capacity for recovery are correlated with the amount of axon terminals spared in the cuneate nucleus. The latter is also closely correlated with the capacity of restoring neuronal responses in somatosensory cortex. Most notable is that the sparing of a small fraction of sensory inputs from the hand may have been sufficient to facilitate the development of compensatory

Conflict of interests

All authors have no conflict of interest.

Acknowledgments

We thank Laura Trice for excellent technical support; Thao Bui for behavioral data analysis; Dr. Mary Baldwin for illustration 12; Dr. Jamie L. Reed for comments on the manuscript; and Dr. Limin Chen for providing three monkeys. This research was supported by NIH grants NS057399 and NS067017 to HXQ; NIH grant NS16446, Christopher and Dana Reeve Foundation to JHK; NIH grant K99 NS079471 and a postdoctoral fellowship from the Canadian Institutes of Health Research to OAG.

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