Spatiotemporal trajectories of reactivation of somatosensory cortex by direct and secondary pathways after dorsal column lesions in squirrel monkeys

Qi, Hui‐Xin; Wang, Feng; Liao, Chia‐Chi; Friedman, Robert M.; Tang, Chaohui; Kaas, Jon H.; Avison, Malcolm J.

doi:10.1016/j.neuroimage.2016.08.015

Cited by 19 publications

(11 citation statements)

References 78 publications

(131 reference statements)

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“…Hantman and Jessell (2010) described a gating circuit for mouse hindlimb proprioceptors in a similar region of the thoracic cord (Clarke's column). This input extent has not been described previously in the monkey, possibly because most earlier studies focused on inputs to the superficial layers, and cut the cord in the horizontal plane (Florence et al, 1988(Florence et al, , 1994Qi et al, 2016), making it difficult to identify labeling in deeper Rexed laminae.…”

Section: Spared Primary Afferents From the Deafferented Digits Sproutmentioning

confidence: 73%

Reorganization of the Primate Dorsal Horn in Response to a Deafferentation Lesion Affecting Hand Function

2020

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The loss of sensory input following a spinal deafferentation injury can be debilitating, and this is especially true in primates when the hand is involved. Although significant recovery of function occurs, little is currently understood about the reorganization of the neuronal circuitry, particularly within the dorsal horn. This region receives primary afferent input from the periphery, and cortical input via the somatosensory subcomponent of the corticospinal tract (S1 CST), and is critically important in modulating sensory transmission, both in normal and lesioned states. To determine how dorsal horn circuitry alters to facilitate recovery post-injury, we used an established deafferentation lesion model (dorsal root/dorsal column) in male monkeys to remove sensory input from just the opposing digits (digits 1-3) of one hand. This results in a deficit in fine dexterity that recovers over several months. Electrophysiological mapping, tract tracing, and immunolabeling techniques were combined to delineate specific changes to dorsal horn input circuitry. Our main findings show that (1) there is complementary sprouting of the primary afferent and S1 CST populations into an overlapping region of the reorganizing dorsal horn; (2) S1 CST and primary afferent inputs connect in different ways within this region to facilitate sensory integration; and (3) there is a loss of larger S1 CST terminal boutons in the affected dorsal horn, but no change in the size profile of the spared/sprouted primary afferent terminal boutons post-lesion. Understanding such changes helps to inform new and targeted therapies that best promote recovery.

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Section: Spared Primary Afferents From the Deafferented Digits Sproutmentioning

confidence: 73%

Reorganization of the Primate Dorsal Horn in Response to a Deafferentation Lesion Affecting Hand Function

2020

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“…Monkeys were scanned in a 9.4T 21-cm narrow-bore Agilent MRI magnet using a 3 cm surface transmit-receive coil secured over primary somatosensory area 3b. For details, see Chen et al, 2012 , Qi and Wang et al, 2016a . Each monkey was anesthetized with isoflurane (0.5–1.1%) delivered by a mixture of N 2 O/O 2 in a 70:30 ratio and mechanically ventilated during MRI scans.…”

Section: Methodsmentioning

confidence: 99%

Longitudinal fMRI measures of cortical reactivation and hand use with and without training after sensory loss in primates

Reed

Wang

et al. 2021

NeuroImage

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In a series of previous studies, we demonstrated that damage to the dorsal column in the cervical spinal cord deactivates the contralateral somatosensory hand cortex and impairs hand use in a reach-to-grasp task in squirrel monkeys. Nevertheless, considerable cortical reactivation and behavioral recovery occurs over the following weeks to months after lesion. This timeframe may also be a window for targeted therapies to promote cortical reactivation and functional reorganization, aiding in the recovery process. Here we asked if and how task specific training of an impaired hand would improve behavioral recovery and cortical reorganization in predictable ways, and if recovery related cortical changes would be detectable using noninvasive functional magnetic resonance imaging (fMRI). We further asked if invasive neurophysiological mapping reflected fMRI results. A reach-to-grasp task was used to test impairment and recovery of hand use before and after dorsal column lesions (DC-lesion). The activation and organization of the affected primary somatosensory cortex (area 3b) was evaluated with two types of fMRI – either blood oxygenation level dependent (BOLD) or cerebral blood volume (CBV) with a contrast agent of monocrystalline iron oxide nanocolloid (MION) – before and after DC-lesion. At the end of the behavioral and fMRI studies, microelectrode recordings in the somatosensory areas 3a, 3b and 1 were used to characterize neuronal responses and verify the somatotopy of cortical reactivations. Our results indicate that even after nearly complete DC lesions, monkeys had both considerable post-lesion behavioral recovery, as well as cortical reactivation assessed with fMRI followed by extracellular recordings. Generalized linear regression analyses indicate that lesion extent is correlated with the behavioral outcome, as well as with the difference in the percent signal change from pre-lesion peak activation in fMRI. Monkeys showed behavioral recovery and nearly complete cortical reactivation by 9–12 weeks post-lesion (particularly when the DC-lesion was incomplete). Importantly, the specific training group revealed trends for earlier behavioral recovery and had higher magnitude of fMRI responses to digit stimulation by 5–8 weeks post-lesion. Specific kinematic measures of hand movements in the selected retrieval task predicted recovery time and related to lesion characteristics better than overall task performance success. For measures of cortical reactivation, we found that CBV scans provided stronger signals to vibrotactile digit stimulation as compared to BOLD scans, and thereby may be the preferred non-invasive way to study the cortical reactivation process after sensory deprivations from digits. When the reactivation of cortex for each of the digits was considered, the reactivation by digit 2 stimulation as measured with microelectrode maps and fMRI maps was best correlated with overall behavioral recovery.

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“…the DCLs. At weeks to months after the DCLs at a high level of the cervical spinal cord, whether incomplete or complete, a variable percentage of the affected hand region in primary somatosensory cortex and higher-order cortex becomes responsive to touch on the hand (2,18,19,21,22). Such somatotopically organized cortical reactivation suggests the existence of spinal cord projections that circumvent the lesion to convey low-threshold tactile inputs from the hand to the Cu after injuries.…”

Section: Secondary-order Spinal Cord Pathway and Cortical Reactivatiomentioning

confidence: 99%

Second-order spinal cord pathway contributes to cortical responses after long recoveries from dorsal column injury in squirrel monkeys

Liao

Reed

et al. 2018

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

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Months after the occurrence of spinal cord dorsal column lesions (DCLs) at the cervical level, neural responses in the hand representation of somatosensory area 3b hand cortex recover, along with hand use. To examine whether the second-order spinal cord pathway contributes to this functional recovery, we injected cholera toxin subunit B (CTB) into the hand representation in the cuneate nucleus (Cu) to label the spinal cord neurons, and related results to cortical reactivation in four squirrel monkeys () at least 7 months after DCL. In two monkeys with complete DCLs, few CTB-labeled neurons were present below the lesion, and few neurons in the affected hand region in area 3b responded to touch on the hand. In two other cases with large but incomplete DCLs, CTB-labeled neurons were abundant below the lesion, and the area 3b hand cortex responded well to tactile stimulation in a roughly somatotopic organization. The proportions of labeled neurons in the spinal cord hand region reflected the extent of cortical reactivation to the hand. Comparing monkeys with short and long recovery times suggests that the numbers of labeled neurons below the lesion increase with time following incomplete DCLs (<95%) but decrease with time after nearly complete DCLs (≥95%). Taken together, these results suggest that the second-order spinal cord pathway facilitates cortical reactivation, likely through the potentiation of persisting tactile inputs from the hand to the Cu over months of postlesion recovery.

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Spatiotemporal trajectories of reactivation of somatosensory cortex by direct and secondary pathways after dorsal column lesions in squirrel monkeys

Cited by 19 publications

References 78 publications

Reorganization of the Primate Dorsal Horn in Response to a Deafferentation Lesion Affecting Hand Function

Reorganization of the Primate Dorsal Horn in Response to a Deafferentation Lesion Affecting Hand Function

Longitudinal fMRI measures of cortical reactivation and hand use with and without training after sensory loss in primates

Second-order spinal cord pathway contributes to cortical responses after long recoveries from dorsal column injury in squirrel monkeys

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