Unilateral brain injury to pregnant rats induces asymmetric neurological deficits in the offspring

Carvalho, Liliana; Brito, Helena M; Lukoyanova, Elena A.; Maia, Gisela H.; Sarkisyan, Daniil; Nosova, Olga; Zhang, Mengliang; Lukoyanov, Nikolay; Bakalkin, Georgy

doi:10.1111/ejn.15243

Cited by 5 publications

(4 citation statements)

References 64 publications

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“…This implies that the brain can alter spinal function through non-neuronal processes (e.g., endocrine signaling). Perhaps more surprising, offspring from pregnant rats that have experienced a brain injury also exhibit a spinally mediated postural asymmetry (Carvalho et al, 2021).…”

Section: Leg Position Gates Whether Nociceptive Stimulation Induce a ...mentioning

confidence: 99%

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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Section: Leg Position Gates Whether Nociceptive Stimulation Induce a ...mentioning

confidence: 99%

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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“…An even more remarkable outcome was obtained when pregnant dams were given a unilateral brain injury. Offspring from injured rats exhibited postural asymmetry and this effect too survived a spinal transection ( Carvalho et al, 2021 ). These spinally-mediated alterations have been linked to distinct patterns of gene expression within the spinal cord.…”

Section: Brain Systems Can Induce a Lasting Modification In Spinal Co...mentioning

confidence: 99%

Updating perspectives on spinal cord function: motor coordination, timing, relational processing, and memory below the brain

Grau,

Hudson,

Johnston

et al. 2024

Front. Syst. Neurosci.

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Those studying neural systems within the brain have historically assumed that lower-level processes in the spinal cord act in a mechanical manner, to relay afferent signals and execute motor commands. From this view, abstracting temporal and environmental relations is the province of the brain. Here we review work conducted over the last 50 years that challenges this perspective, demonstrating that mechanisms within the spinal cord can organize coordinated behavior (stepping), induce a lasting change in how pain (nociceptive) signals are processed, abstract stimulus–stimulus (Pavlovian) and response-outcome (instrumental) relations, and infer whether stimuli occur in a random or regular manner. The mechanisms that underlie these processes depend upon signal pathways (e.g., NMDA receptor mediated plasticity) analogous to those implicated in brain-dependent learning and memory. New data show that spinal cord injury (SCI) can enable plasticity within the spinal cord by reducing the inhibitory effect of GABA. It is suggested that the signals relayed to the brain may contain information about environmental relations and that spinal cord systems can coordinate action in response to descending signals from the brain. We further suggest that the study of stimulus processing, learning, memory, and cognitive-like processing in the spinal cord can inform our views of brain function, providing an attractive model system. Most importantly, the work has revealed new avenues of treatment for those that have suffered a SCI.

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“…The developing nervous system is sensitive to environmental influences that could affect pregnant females. Several environmental effects are transmitted to the next generation and cause neuropsychiatric disorders (reviewed in [ 143 ]. Intergenerational transmission has been reported for stress, anxiety, cocaine use, and enhanced synaptic plasticity.…”

Section: The Neuroendocrine “Cross Association” Phenomenonmentioning

confidence: 99%

“…By analogy, unilateral TBI and stroke in pregnant females may affect the developing neuroendocrine system and through the intergenerational mechanism cause neurological deficits in the offspring. This hypothesis has been tested with the HL-PA model [ 143 ]. The main finding was that the unilateral ablation injury of the hindlimb sensorimotor cortex in pregnant rats resulted in formation of HL-PA in the offspring.…”

Section: The Neuroendocrine “Cross Association” Phenomenonmentioning

confidence: 99%

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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Unilateral brain injury to pregnant rats induces asymmetric neurological deficits in the offspring

Cited by 5 publications

References 64 publications

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

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

Updating perspectives on spinal cord function: motor coordination, timing, relational processing, and memory below the brain

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

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