Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

McVea, David A.; Mohajerani, Majid H.; Murphy, Timothy H.

doi:10.1523/jneurosci.1322-12.2012

Cited by 47 publications

(42 citation statements)

References 72 publications

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“…Twitch movements may be particularly well suited to this task because, unlike wake movements, they are produced discretely against a background of muscle atonia, both of which enhance signal-to-noise ratio [19]. Our results further suggest that the high fidelity of twitching depends upon the suspension of corollary discharge mechanisms, providing the infant with ideal conditions for activity-dependent development of the spinal cord [35], cerebellum [23], and forebrain [20–22, 36]. The information provided by twitching limbs may also enable the construction and calibration of internal models and predictive codes, which are thought to be essential for flexible and efficient sensorimotor control throughout the lifespan [37–39].…”

Section: Resultsmentioning

confidence: 83%

Self-Generated Movements with “Unexpected” Sensory Consequences

2014

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SUMMARY The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.

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Section: Resultsmentioning

confidence: 83%

Self-Generated Movements with “Unexpected” Sensory Consequences

2014

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“…A map shift in the mediolateral axis is consistent with reorganization within contiguous areas of the motor cortex, while anteroposterior shifts indicate recruitment of neighboring nonprimary motor areas such as the premotor cortex or postcentral cortex [34,35]. Elegant imaging techniques by the laboratories of Dijkhuizen [36,37] and Murphy [38] have confirmed significant functional magnetic resonance imaging (fMRI) or voltage-sensitive dye responses in the infarct periphery ipsilesional to the stroke in animals. Equally elegant labeling of sprouting axons after stroke in the + ATPase.…”

Section: Introductionmentioning

confidence: 80%

The Epigenetics of Stroke Recovery and Rehabilitation: From Polycomb to Histone Deacetylases

et al. 2013

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Classical de-afferentation studies, as well as experience-dependent visual plasticity paradigms, have confirmed that both the developing and adult nervous system are capable of unexpected levels of plasticity. This capacity is underscored by the significant spontaneous recovery that can occur in patients with mild-to-moderate impairment following stroke. An evolving model is that an interaction of biological and environmental factors during all epochs post-stroke influences the extent and quality of this plasticity. Here, we discuss data that have implicated specific epigenetic proteins as integrators of environmental influences in 3 aspects of stroke recovery: spontaneous impairment reduction in humans; peri-infarct rewiring in animals as a paradigm for developing therapeutically-driven impairment reduction beyond natural spontaneous recovery; and, finally, classical hippocampal learning and memory paradigms that are theoretically important in skill acquisition for both impairment reduction and compensatory strategies in the rehabilitation setting. Our discussion focuses primarily on B lymphoma Mo-MLV1 insertion region proteins of the polycomb repressive complex, alpha thalassemia/mental retardation syndrome X-linked chromatin remodeling factors, and the best known and most dynamic gene repressors, histone deacetylases. We will highlight exciting current data associated with these proteins and provide promising speculation about how they can be manipulated by drugs, biologics, or noninvasive stimulation for stroke recovery.

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“…In the adult brain, complex bilateral patterns of brain-wide spontaneous neural activity were observed, consistent with the results of previous studies using voltagesensitive dyes in the adult brain, and interpreted to represent brain-wide network activity. 15,34,37,39 In the same mice, hemodynamics across development mirrored those seen in rats: No localized increases in blood flow were observed at P7, despite the presence of strong, localized neural activity. By P10, only small correlated increases in blood flow were observed.…”

Section: Introductionmentioning

confidence: 62%

Neurovascular coupling develops alongside neural circuits in the postnatal brain

Kozberg

Hillman

2016

Neurogenesis

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In the adult brain, increases in local neural activity are accompanied by increases in regional blood flow. This relationship between neural activity and hemodynamics is termed neurovascular coupling and provides the blood flow-dependent contrast detected in functional magnetic resonance imaging (fMRI). Neurovascular coupling is commonly assumed to be consistent and reliable from birth; however, numerous studies have demonstrated markedly different hemodynamics in the early postnatal brain. Our recent study in J. Neuroscience examined whether different hemodynamics in the immature brain are driven by differences in the underlying spatiotemporal properties of neural activity during this period of robust neural circuit expansion. Using a novel wide-field optical imaging technique to visualize both neural activity and hemodynamics in the mouse brain, we observed longer duration and increasingly complex patterns of neural responses to stimulus as cortical connectivity developed over time. However, imaging of brain blood flow, oxygenation, and metabolism in the same mice demonstrated an absence of coupled blood flow responses in the newborn brain. This lack of blood flow coupling was shown to lead to oxygen depletions following neural activations -depletions that may affect the duration of sustained neural responses and could be important to the vascular patterning of the rapidly developing brain. These results are a step toward understanding the unique neurovascular and neurometabolic environment of the newborn brain, and provide new insights for interpretation of fMRI BOLD studies of early brain development. Local neural activity in the adult brain leads to large increases in local blood flow. These increases in blood flow seemingly overcompensate for local oxygen consumption, leading to increases in the local concentration of both oxygenated (HbO) and total hemoglobin (HbT) and decreases in deoxygenated hemoglobin (HbR) due to a washout effect. 21,22,33 This decrease in the concentration of HbR is the basis of the fMRI BOLD response and it has been commonly assumed that these responses are in place and consistent from birth. Although some neonatal fMRI and near infrared spectroscopy (NIRS) studies have reported adult-like responses, 3,31,49 many studies in both humans and rodent models have reported differences in hemodynamic responses in the early postnatal brain compared to adults. 1,9,26,38,57 Such findings have raised doubts over the use of hemodynamic-dependent imaging modalities to study developing neural connectivity. Our recent study in J.Neuroscience is the first to image neural and hemodynamic activity simultaneously across the early postnatal mouse cortex, providing a unique look at the formation of neural circuitry alongside the establishment of neurovascular coupling.Our work on this subject began with a study in rats at postnatal days 12-23 (P12-23), which demonstrated that somatosensory (hindpaw) stimulation does not evoke increases in local blood flow at P12. 26At around P15, small, immatur...

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Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

Cited by 47 publications

References 72 publications

Self-Generated Movements with “Unexpected” Sensory Consequences

Self-Generated Movements with “Unexpected” Sensory Consequences

The Epigenetics of Stroke Recovery and Rehabilitation: From Polycomb to Histone Deacetylases

Neurovascular coupling develops alongside neural circuits in the postnatal brain

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