Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury

Lukoyanov, Nikolay; Watanabe, Hiroyuki; Carvalho, Liliana; Кононенко, О.; Sarkisyan, Daniil; Zhang, Mengliang; Andersen, Marlene Storm; Lukoyanova, Elena A.; Galatenko, Vladimir; Tonevitsky, Alex; Bazov, Igor; Iakovleva, Tatiana; Schouenborg, Jens; Bakalkin, Georgy

doi:10.7554/elife.65247

Cited by 14 publications

(88 citation statements)

References 146 publications

(240 reference statements)

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“…Our previous (Lukoyanov et al, 2021) and present studies provide evidence that the left-right side-specific humoral signaling mediates the effects of UBI on the formation of HL-PA, asymmetry in passive hindlimb musculo-articular resistance to stretching and withdrawal reflexes, and asymmetric changes in gene expression patterns in the lumbar spinal cord. Hypothetically, the paravertebral chain of sympathetic ganglia, which is the remaining neural connection between the rostral and caudal parts of the transected spinal cord, may convey supraspinal signals to the muscle vasculature and through this mechanism may differentially affect ipsi- and contralesional muscles.…”

Section: Discussionsupporting

confidence: 67%

“…A critical evidence that the sympathetic system does not mediate signals from injured brain to the lumbar spinal cord is provide by the present study; the hindlimb postural asymmetry and asymmetry in their musculo-articular resistance to stretch develop in rats with complete transection of the cervical spinal cord that was at the level rostral to the localization of preganglionic sympathetic neurons in the T1 - L2/3 segments. Experiments with hypophysectomized rats, “pathological” serum and neurohormones that induce HL-PA provide evidence for the humoral pathway in rats with transected spinal cord (Lukoyanov et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…The HL-PA value and the side of the flexed limb were assessed as described elsewhere (Lukoyanov et al, 2021; Watanabe et al, 2020; Zhang et al, 2020). Briefly, the measurements were performed under pentobarbital (60 mg/kg, i.p.).…”

Section: Methodsmentioning

confidence: 99%

“…In the hands-off method, silk threads were glued to the nails of the middle three toes of each hindlimb, and their other ends were tied to one of two hooks attached to the movable platform that was operated by a micromanipulator constructed in the laboratory (Lukoyanov et al, 2021). To reduce potential friction between the hindlimbs and the surface with changes in their position during stretching and after releasing them, the bench under the rat was covered with plastic sheet and the movable platform was raised up to form a 10° angle between the threads and the bench surface.…”

Section: Methodsmentioning

confidence: 99%

“…Early studies suggested that in addition to the descending neural tracts the contralesional effects of brain injury may be mediated by an extra-spinal mechanism (Cope et al, 1980; Wolpaw and Lee, 1989). To test this hypothesis, the descending neural tracts were disabled by complete transection of the thoracic spinal cord before the brain injury was performed (Lukoyanov et al, 2021). In spite of prior spinal cord transection, a unilateral injury of the hindlimb sensorimotor cortex resulted in formation of HL-PA with contralateral flexion, and asymmetric changes in hindlimb withdrawal reflexes and expression patterns of neuroplasticity-related genes in the lumbar spinal cord.…”

Section: Introductionmentioning

confidence: 99%

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Humoral signaling-mediated effects of unilateral brain injury: differences in the left-right sided afferent responses

Watanabe

Kobikov²,

Sarkisyan

et al. 2022

Preprint

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Disruption of neural tracts descending from the brain to the spinal cord after brain trauma and stroke causes postural and sensorimotor deficits. We previously showed that unilateral lesion to the sensorimotor cortex in rats with completely transected thoracic spinal cord produced asymmetry in hindlimb posture and withdrawal reflexes. Supraspinal signals to hindlimb muscles may be transmitted through the paravertebral chain of sympathetic ganglia that remain intact after the transection. We here demonstrated that prior transection of the spinal cord at the cervical level that was rostrally to segments with preganglionic sympathetic neurons, did not abolish formation of asymmetry in hindlimb posture and musculo-articular resistance to stretch after unilateral brain injury. Thus not the sympathetic system but humoral signals may mediate the effects of brain injury on the lumbar spinal circuits. The asymmetric responses in rats with transected spinal cords were eliminated by bilateral lumbar dorsal rhizotomy after the left-side brain injury, but resistant to deafferentation after the right-side brain lesion. Two mechanisms, one dependent on and one independent of afferent input may account for asymmetric hindlimb motor responses. Resistance to deafferentation may be due to sustained stretch- and effort-unrelated muscle contractions that is often observed in patients with central lesions. Left-right asymmetry is unusual feature of these mechanisms that both are activated by humoral signals.

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Section: Discussionsupporting

confidence: 67%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Humoral signaling-mediated effects of unilateral brain injury: differences in the left-right sided afferent responses

Watanabe

Kobikov²,

Sarkisyan

et al. 2022

Preprint

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The left–right side-specific endocrine signaling in the effects of brain lesions: questioning of the neurological dogma

Bakalkin

2022

Cell. Mol. Life Sci.

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Each cerebral hemisphere is functionally connected to the contralateral side of the body through the decussating neural tracts. The crossed neural pathways set a basis for contralateral effects of brain injury such hemiparesis and hemiplegia as it has been already noted by Hippocrates. Recent studies demonstrated that, in addition to neural mechanisms, the contralateral effects of brain lesions are mediated through the humoral pathway by neurohormones that produce either the left or right side-specific effects. The side-specific humoral signaling defines whether the left or right limbs are affected after a unilateral brain injury. The hormonal signals are released by the pituitary gland and may operate through their receptors that are lateralized in the spinal cord and involved in the side-specific control of symmetric neurocircuits innervating the left and right limbs. Identification of features and a proportion of neurological deficits transmitted by neurohormonal signals vs. those mediated by neural pathways is essential for better understanding of mechanisms of brain trauma and stroke and development of new therapies. In a biological context, the left–right side-specific neuroendocrine signaling may be fundamental for the control of the left- and right-sided processes in bilaterally symmetric animals.

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Behavioral studies of spinal conditioning: The spinal cord is smarter than you think it is.

Grau¹,

Hudson²,

Tarbet³

et al. 2022

Journal of Experimental Psychology: Animal Learning and Cogniti

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In 1988 Robert Rescorla published an article in the Annual Review of Neuroscience that addressed the circumstances under which learning occurs, some key methodological issues, and what constitutes an example of learning. The article has inspired a generation of neuroscientists, opening the door to a wider range of learning phenomena. After reviewing the historical context for his article, its key points are briefly reviewed. The perspective outlined enabled the study of learning in simpler preparations, such as the spinal cord. The period after 1988 revealed that pain (nociceptive) stimuli can induce a lasting sensitization of spinal cord circuits, laying down a kind of memory mediated by signal pathways analogous to those implicated in brain dependent learning and memory. Evidence suggests that the spinal cord is sensitive to instrumental response-outcome (R-O) relations, that learning can induce a peripheral modification (muscle memory) that helps maintain the learned response, and that learning can promote adaptive plasticity (a form of metaplasticity). Conversely, exposure to uncontrollable stimulation disables the capacity to learn. Spinal cord neurons can also abstract that stimuli occur in a regular (predictable) manner, a capacity that appears linked to a neural oscillator (central pattern generator). Disrupting communication with the brain has been shown to transform how GABA affects neuronal function (an example of ionic plasticity), releasing a brake that enables plasticity. We conclude by presenting a framework for understanding these findings and the implications for the broader study of learning.

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Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury

Cited by 14 publications

References 146 publications

Humoral signaling-mediated effects of unilateral brain injury: differences in the left-right sided afferent responses

Humoral signaling-mediated effects of unilateral brain injury: differences in the left-right sided afferent responses

The left–right side-specific endocrine signaling in the effects of brain lesions: questioning of the neurological dogma

Behavioral studies of spinal conditioning: The spinal cord is smarter than you think it is.

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