Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat

Ngai, Al C.; Jolley, Matthew A.; D’Ambrosio, Raimondo; Meno, Joseph R.; Winn, H. Richard

doi:10.1016/s0006-8993(99)01649-2

Cited by 112 publications

(86 citation statements)

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“…Brinker et al (59) were able to demonstrate a close correlation between SEP amplitude and BOLD signal amplitude during forepaw stimulation, which was later confirmed by Ogawa and colleagues (60). Other studies have shown that, although SEP amplitude decreases with increasing stimulation frequency, the CBF does not correlate with the amplitude of the SEP, but with the integrated neuronal activity (61)(62)(63)(64). Extensive studies further show that this neurovascular coupling is described by a non-linear relationship, which can, however, be approximated as roughly linear within a narrow range (48,65).…”

Section: Electrical Brain Activity and The Haemodynamic Responsementioning

confidence: 98%

Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

et al. 2007

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This review aims to make the reader aware of the potential of functional MRI (fMRI) in brain activation studies in small animal models. As small animals generally require anaesthesia for immobilization during MRI protocols, this is believed to be a serious limitation to the type of question that can be addressed with fMRI. We intend to introduce a fresh view with an in-depth overview of the surprising number of fMRI applications in a wide range of important research domains in neuroscience. These include the pathophysiology of brain functioning, the basic science of activity, and functional connectivity of different sensory circuits, including sensory brain mapping, the challenges when studying the hypothalamus as the major control centre in the central nervous system, and the limbic system as neural substrate for emotions and reward. Finally the contribution of small animal fMRI research to cognitive neuroscience is outlined. This review avoids focusing exclusively on traditional small laboratory animals such as rodents, but rather aims to broaden the scope by introducing alternative lissencephalic animal models such as songbirds and fish, as these are not yet well recognized as neuroimaging study subjects. These models are well established in many other neuroscience disciplines, and this review will show that their investigation with in vivo imaging tools will open new doors to cognitive neuroscience and the study of the autonomous nervous system in experimental animals.

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Section: Electrical Brain Activity and The Haemodynamic Responsementioning

confidence: 98%

Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

et al. 2007

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“…Furthermore, most of the optical studies performed using electrical stimulation varied either in frequency (Ngai et al, 1999;Matsuura and Kanno, 2001;Martindale et al, 2003; -3 - while maintaining a fixed current strength (Brinker et al, 1999;Van Camp et al, 2006;Goloshevsky et al, 2007;Huttunen et al, 2008;Sanganahalli et al, 2009), and few fMRI studies have comprehensively investigated this relationship at different stimulus frequencies and currents.…”

Section: Introductionmentioning

confidence: 99%

“…Although most of the human fMRI studies employ the event-related task design that has a short stimulus duration, animal studies generally investigate the relationship between BOLD signals and evoked potentials with a stimulus duration of several tens of seconds (Brinker et al, 1999;Van Camp et al, 2006;Goloshevsky et al, 2007;Huttunen et al, 2008;Sanganahalli et al, 2009). Unlike BOLD studies, numerous optical studies performed using laser Doppler flowmetry (LDF) (Ngai et al, 1999;Matsuura and Kanno, 2001;Ureshi et al, 2004Ureshi et al, , 2005 and optical imaging (Devor et al, 2003;Martindale et al, 2003;Sheth et al, 2003Sheth et al, , 2004Jones et al, 2004;Hewson-Stoate et al, 2005;Martin et al, 2006) have investigated the hemodynamic responses such as CBF and deoxygenated hemoglobin changes to neuronal activity in the rat cortex with a short stimulus duration (2-5 s) (Matsuura and Kanno, 2001;Martindale et al, 2003;Sheth et al, 2003Sheth et al, , 2004Jones et al, 2004;Ureshi et al, 2004Ureshi et al, , 2005Hewson-Stoate et al, 2005;Martin et al, 2006). Thus, an animal fMRI study with short stimulus duration is expected to bridge the results of the optical studies using short stimulus durations and those of the BOLD studies using long stimulus durations.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, most of the optical studies performed using electrical stimulation varied either in frequency (Ngai et al, 1999;Matsuura and Kanno, 2001;Martindale et al, 2003; -3 -2003; Ureshi et al, 2004), or current (Jones et al, 2004, Ureshi et al, 2005, or both (Sheth et al, 2004;Hewson-Stoate et al, 2005). Animal fMRI studies on somatosensory activation investigated the relationship between BOLD signals and neuronal activities by changing the stimulus frequency while maintaining a fixed current strength (Brinker et al, 1999;Van Camp et al, 2006;Goloshevsky et al, 2007;Huttunen et al, 2008;Sanganahalli et al, 2009), and few fMRI studies have comprehensively investigated this relationship at different stimulus frequencies and currents.…”

Section: Introductionmentioning

confidence: 99%

“…Unlike BOLD studies, numerous optical studies performed using laser Doppler flowmetry (LDF) (Ngai et al, 1999;Matsuura and Kanno, 2001;Ureshi et al, 2004Ureshi et al, , 2005 and optical imaging (Devor et al, 2003;Martindale et al, 2003;Sheth et al, 2003Sheth et al, , 2004Jones et al, 2004;Hewson-Stoate et al, 2005;Martin et al, 2006) have investigated the hemodynamic responses such as CBF and deoxygenated hemoglobin changes to neuronal activity in the rat cortex with a short stimulus duration (2-5 s) (Matsuura and Kanno, 2001;Martindale et al, 2003;Sheth et al, 2003Sheth et al, , 2004Jones et al, 2004;Ureshi et al, 2004Ureshi et al, , 2005Hewson-Stoate et al, 2005;Martin et al, 2006). Thus, an animal fMRI study with short stimulus duration is expected to bridge the results of the optical studies using short stimulus durations and those of the BOLD studies using long stimulus durations.Furthermore, most of the optical studies performed using electrical stimulation varied either in frequency (Ngai et al, 1999;Matsuura and Kanno, 2001;Martindale et al, 2003; -3 - while maintaining a fixed current strength (Brinker et al, 1999;Van Camp et al, 2006;Goloshevsky et al, 2007;Huttunen et al, 2008;Sanganahalli et al, 2009), and few fMRI studies have comprehensively investigated this relationship at different stimulus frequencies and currents.Thus, the present study aimed to investigate the relationship between BOLD signals and neuronal activities in the somatosensory cortex of anesthetized rats for forepaw electrical stimulation at a short duration of 4 s by changing both frequencies (1-10 Hz) and currents (0.5-2.0 mA). BOLD signals with a spin-echo echo planar imagining (EPI) sequence at 7 T and scalp-based somatosensory evoked potentials (SEP) were obtained from individual rats.…”

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Comprehensive correlation between neuronal activity and spin-echo blood oxygenation level-dependent signals in the rat somatosensory cortex evoked by short electrical stimulations at various frequencies and currents

Kida

Yamamoto

2010

Brain Research

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It is essential to elucidate the relationship between blood oxygenation level-dependent (BOLD) signals and neuronal activity for the interpretation of the functional magnetic resonance imaging (fMRI) signals; this relationship has been quantitatively investigated by animal studies measuring evoked potentials as indices of neuronal activity. Although most human fMRI studies employ the event-related task design, in which the stimulus duration is short, few studies have investigated the relationship between BOLD signals and evoked potentials at short stimulus durations. The present study investigated this relationship in the somatosensory cortex of anesthetized rats by using electrical forepaw stimulation at a short duration of 4 s and comprehensively analyzed it at different frequencies (1-10 Hz) and currents (0.5-2.0 mA). Somatosensory evoked potential (SEP) responses were measured at the scalp using silver ball electrodes. The sum of the peak-to-peak amplitude (ΣSEP) and average SEP (avg. SEP) responses were calculated. BOLD signals were obtained using a spin-echo echo-planar imaging sequence at 7 T. The relationship between the avg.SEP and BOLD signals varied with frequency, whereas that between ΣSEP and BOLD signals showed a significant correlation at varying frequencies and currents. In particular, the relationship between ΣSEP and ΣBOLD, which is the sum of the BOLD signals obtained at each time point reflecting the area under the BOLD response curves, mostly converged, irrespective of the frequency. Our results suggest that ΣBOLD obtained using a spin-echo sequence reflects the neural activity as quantified by ΣSEP, which was determined at different frequencies and currents. Section: Regulatory SystemsKeywords: BOLD; fMRI; Forepaw; Neurovascular coupling; SEP Abbreviations: BOLD, blood oxygenation level-dependent; CBF, cerebral blood flow; CMRO 2 , cerebral metabolic rate of oxygen consumption; EPI, echo planar imagining; TE, echo time; fMRI, functional magnetic resonance imaging; LDF, laser Doppler flowmetry; SEP, somatosensory evoked potential; T 2 , transverse relaxation time -2 - IntroductionFunctional magnetic resonance imaging (fMRI) based on blood oxygenation level-dependent (BOLD) effect has been widely used in neuroscience and psychology to study brain function. fMRI reflects cerebral hemodynamic changes, and its signals have been interpreted by assuming a neuronal hemodynamic response (Friston et al., 1995) based on the 19 th century hypothesis of Roy and Sherrington that neuronal activity induces an increase in the regional cerebral blood flow (CBF) (Roy and Sherrington, 1890). Thus, fMRI is an indirect method for assessing neuronal activity. Therefore, it is essential to elucidate the relationship between BOLD signals and neuronal activity for interpreting the fMRI signals; this relationship has been investigated mainly by animal studies measuring evoked potentials as indices of the neuronal activity in the somatosensory cortex (Brinker et al., 1999;Van Camp et al., 2006;Goloshevsk...

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Functional Neuroimaging of Nociceptive and Pain‐Related Activity in the Spinal Cord and Brain: Insights From Neurovascular Coupling Studies

Paquette

Jeffrey-Gauthier

Leblond

et al. 2018

The Anatomical Record

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Spinal cord and brain processes underlie pain perception, which produces systemic cardiovascular changes. In turn, the autonomic nervous system regulates vascular function in the spinal cord and brain in order to adapt to these systemic changes, while neuronal activity induces local vascular changes. Thus, autonomic regulation and pain processes in the brain and spinal cord are tightly linked and interrelated. The objective of this topical review is to discuss work on neurovascular coupling during nociceptive processing in order to highlight supporting evidence and limitations for the use of cerebral and spinal fMRI to investigate pain mechanisms and spinal nociceptive processes. Work on functional neuroimaging of pain is presented and discussed in relation to available neurovascular coupling studies and related issues. Perspectives on future work are also discussed with an emphasis on differences between the brain and the spinal cord and on different approaches that may be useful to improve current methods, data analyses and interpretation. In summary, this review highlights the lack of data on neurovascular coupling during nociceptive stimulation and indicates that hemodynamic and BOLD responses measured with fMRI may be biased by nonspecific vascular changes. Future neuroimaging studies on nociceptive and pain-related processes would gain further understanding of neurovascular coupling in the brain and spinal cord and should take into account the effects of systemic vascular changes that may affect hemodynamic responses. Anat Rec, 301:1585-1595, 2018. © 2018 Wiley Periodicals, Inc.

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Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat

Cited by 112 publications

References 22 publications

Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

Comprehensive correlation between neuronal activity and spin-echo blood oxygenation level-dependent signals in the rat somatosensory cortex evoked by short electrical stimulations at various frequencies and currents

Functional Neuroimaging of Nociceptive and Pain‐Related Activity in the Spinal Cord and Brain: Insights From Neurovascular Coupling Studies

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