Cocaine administration produces a protracted decoupling of neural and haemodynamic responses to intense sensory stimuli

Berwick, Jason; Devonshire, Ian M.; Martindale, A.J.; Johnston, Dave; Zheng, Ying; Kennerley, Aneurin J.; Overton, Paul G.; Mayhew, John E. W.

doi:10.1016/j.neuroscience.2004.12.021

Cited by 9 publications

(10 citation statements)

References 34 publications

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“…Similar differences are evident between the awake data reported here and other studies using anaesthetized animals (e.g. Berwick et al. , 2005; Kennerley et al.…”

Section: Discussionsupporting

confidence: 91%

“…where 0 denotes baseline value and the parameters cr and ct permit the scaling of OIS-measured fractional changes in Hbr and Hbt, derived from the tissue as a whole (including venous, arterial and capillary compartments, hereafter the 'mixed' compartment), to changes in the venous compartment only. This method has been used previously to estimate CMRO 2 changes in both human (Boas et al, 2003;Durduran et al, 2004) and anaesthetized animal studies (Jones et al, , 2005Sheth et al, 2004;Berwick et al, 2005;Dunn et al, 2005), and was employed here on the awake animal data.…”

Section: Estimation Of Cerebral Metabolic Rate Of Oxygenmentioning

confidence: 99%

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Haemodynamic and neural responses to hypercapnia in the awake rat

Martin

Jones

Martindale

et al. 2006

Eur J of Neuroscience

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The relationship between localized changes in brain activity and metabolism, and the blood oxygenation level-dependent (BOLD) signal used in functional magnetic resonance imaging studies is not fully understood. One source of complexity is that stimulus-elicited changes in the BOLD signal arise both from changes in oxygen consumption due to increases in activity and purely 'haemodynamic' changes such as increases in cerebral blood flow. It is well established that robust cortical haemodynamic changes can be elicited by increasing the concentration of inspired CO(2) (inducing hypercapnia) and it is widely believed that these haemodynamic changes occur without significant effects upon neural activity or cortical metabolism. Hypercapnia is therefore commonly used as a calibration condition in functional magnetic resonance imaging studies to enable estimation of oxidative metabolism from subsequent stimulus-evoked functional magnetic resonance imaging BOLD signal changes. However, there is little research that has investigated in detail the effects of hypercapnia upon all components of the haemodynamic response (changes in cerebral blood flow, volume and oxygenation) in addition to recording neural activity. In awake animals, we used optical and electrophysiological techniques to measure cortical haemodynamic and field potential responses to hypercapnia (60 s, 5% CO(2)). The main findings are that firstly, in the awake rat, the temporal structure of the haemodynamic response to hypercapnia differs from that reported previously in anaesthetized preparations in that the response is more rapid. Secondly, there is evidence that hypercapnia alters ongoing neural activity in awake rats by inducing periods of cortical desynchronization and this may be associated with changes in oxidative metabolism.

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“…Similar differences are evident between the awake data reported here and other studies using anaesthetized animals (e.g. Berwick et al. , 2005; Kennerley et al.…”

Section: Discussionsupporting

confidence: 91%

Section: Estimation Of Cerebral Metabolic Rate Of Oxygenmentioning

confidence: 99%

Haemodynamic and neural responses to hypercapnia in the awake rat

Martin

Jones

Martindale

et al. 2006

Eur J of Neuroscience

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“…Furthermore, Devonshire et al53 demonstrated that the neuronal response as measured by summed field potential to intense somatosensory (whisker) stimulation after cocaine was enhanced in barrel cortex. In parallel with the electrophysiological recordings, they also measured the hemodynamic responses during somatosensory stimulation using a combination of optical and BOLD fMRI techniques 56. The data demonstrated that, because cocaine in itself increased the baseline cerebral blood flow and BOLD signals over time in the somatosensory cortex, the ensuing responses recorded were not accurately reflecting the enhanced neuronal response 56.…”

Section: Discussionmentioning

confidence: 99%

“…In parallel with the electrophysiological recordings, they also measured the hemodynamic responses during somatosensory stimulation using a combination of optical and BOLD fMRI techniques 56. The data demonstrated that, because cocaine in itself increased the baseline cerebral blood flow and BOLD signals over time in the somatosensory cortex, the ensuing responses recorded were not accurately reflecting the enhanced neuronal response 56. We observed that LIDO enhanced the fMRI BOLD activation in somatosensory cortex in response to the acute noxious stimulation and, because LIDO unlike cocaine does not seem to affect baseline cerebral hemodynamics to the same degree,57 we suggest therefore that the fMRI enhancement observed truly represents enhanced neuronal activation.…”

Section: Discussionmentioning

confidence: 99%

The Effect of Intravenous Lidocaine on Brain Activation During Non-Noxious and Acute Noxious Stimulation of the Forepaw: A Functional Magnetic Resonance Imaging Study in the Rat

Luo

Yu²,

Smith³

et al. 2009

Anesthesia &Amp; Analgesia

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BACKGROUND Lidocaine can alleviate acute as well as chronic neuropathic pain at very low plasma concentrations in humans and laboratory animals. The mechanism(s) underlying lidocaine’s analgesic effect when administered systemically is poorly understood but clearly not related to interruption of peripheral nerve conduction. Other targets for lidocaine’s analgesic action(s) have been suggested, including sodium channels and other receptor sites in the central rather than peripheral nervous system. To our knowledge, the effect of lidocaine on the brain’s functional response to pain has never been investigated. Here, we therefore characterized the effect of systemic lidocaine on the brain’s response to innocuous and acute noxious stimulation in the rat using functional magnetic resonance imaging (fMRI). METHODS Alpha-chloralose anesthetized rats underwent fMRI to quantify brain activation patterns in response to innocuous and noxious forepaw stimulation before and after IV administration of lidocaine. RESULTS Innocuous forepaw stimulation elicited brain activation only in the contralateral primary somatosensory (S1) cortex. Acute noxious forepaw stimulation induced activation in additional brain areas associated with pain perception, including the secondary somatosensory cortex (S2), thalamus, insula and limbic regions. Lidocaine administered at IV doses of either 1 mg/kg, 4 mg/kg or 10 mg/kg did not abolish or diminish brain activation in response to innocuous or noxious stimulation. In fact, IV doses of 4 mg/kg and 10 mg/kg lidocaine enhanced S1 and S2 responses to acute nociceptive stimulation, increasing the activated cortical volume by 50%–60%. CONCLUSION The analgesic action of systemic lidocaine in acute pain is not reflected in a straightforward interruption of pain-induced fMRI brain activation as has been observed with opioids. The enhancement of cortical fMRI responses to acute pain by lidocaine observed here has also been reported for cocaine. We recently showed that both lidocaine and cocaine increased intra-cellular calcium concentrations in cortex, suggesting that this pharmacological effect could account for the enhanced sensitivity to somatosensory stimulation. As our model only measured physiological acute pain, it will be important to also test the response of these same pathways to lidocaine in a model of neuropathic pain to further investigate lidocaine’s analgesic mechanism of action.

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“…Noninvasive imaging techniques such as positron emission tomography (London et al, 1990;Volkow et al, 1992Volkow et al, , 1996 and magnetic resonance imaging (MRI) (Breiter et al, 1997;Breiter and Rosen, 1999;Mandeville et al, 2001; Lee et al, 2003) have been used to investigate the effects of cocaine in the human brain and in animals. Optical techniques have also been used to monitor the cerebrovascular and functional effects of cocaine in animals (Stankovic et al, 1998;Devonshire et al, 2004;Berwick et al, 2005). One advantage of optical technology is that it can concurrently detect oxyhemoglobin and deoxyhemoglobin, thereby distinguishing changes in the total hemoglobin concentration and oxygenation (Jobsis, 1977;Chance et al, 1988;Cope and Delpy, 1988).…”

Section: Introductionmentioning

confidence: 99%

Cocaine Increases the Intracellular Calcium Concentration in Brain Independently of Its Cerebrovascular Effects

Du¹,

Yu²,

Volkow³

et al. 2006

J. Neurosci.

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Cocaine abuse increases the risk of life-threatening neurological complications such as strokes and seizures. Although the vasoconstricting properties of cocaine underlie its cerebrovascular effects, the mechanisms underlying its neurotoxicity remain incompletely understood. ] i in the brain. The effects of cocaine were compared with those of methylphenidate, which has similar catecholaminergic effects as cocaine (except for serotonin increases) but no local anesthetic properties, and of lidocaine, which has similar local anesthetic effects as cocaine but is devoid of catecholaminergic actions. To control for the hemodynamic effects of cocaine, we assessed the effects of cocaine in animals in which normal blood pressure was maintained by infusion of phenylephrine, and we also measured the effects of transient hypotension (mimicking that induced by cocaine). We show that cocaine induced significant increases (ϳ10 -15%) in [Ca 2ϩ ] i that were independent of its hemodynamic effects and of the anesthetic used (isofluorance or ␣-chloralose).

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Cocaine administration produces a protracted decoupling of neural and haemodynamic responses to intense sensory stimuli

Cited by 9 publications

References 34 publications

Haemodynamic and neural responses to hypercapnia in the awake rat

Haemodynamic and neural responses to hypercapnia in the awake rat

The Effect of Intravenous Lidocaine on Brain Activation During Non-Noxious and Acute Noxious Stimulation of the Forepaw: A Functional Magnetic Resonance Imaging Study in the Rat

Cocaine Increases the Intracellular Calcium Concentration in Brain Independently of Its Cerebrovascular Effects

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