Imaging of temperature dependent hemodynamics in the rat sciatic nerve by functional photoacoustic microscopy

BackgroundVascular hemodynamics is central to the regulation of neuro-metabolism and plays important roles in peripheral nerves diseases and their prevention. However, at present there are only a few techniques capable of directly measuring peripheral nerve vascular hemodynamics.MethodHere, we investigate the use of dark-field functional photoacoustic microscopy (fPAM) for intrinsic visualizing of the relative hemodynamics of the rat sciatic nerve in response to localized temperature modulation (i.e., cooling and rewarming).Results and conclusionOur main results show that the relative functional total hemoglobin concentration (HbT) is more significantly correlated with localized temperature changes than the hemoglobin oxygen saturation (SO2) changes in the sciatic nerve. Our study also indicates that the relative HbT changes are better markers of neuronal activation than SO2 during nerve temperature changes. Our results show that fPAM is a promising candidate for in vivo imaging of peripheral nerve hemodynamics without the use of contrast agents. Additionally, this technique may shed light on the neuroprotective effect of hypothermia on peripheral nerves by visualizing their intrinsic hemodynamics.

[1]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Greve,et al.  Digital Blood Flow in Cooled and Contralateral Finger in Patients with Raynaud's Phenomenon. Comparative Measurements Between Photoelectrical Plethysmography and Laser Doppler Flowmetry , 1992, Angiology.

[3]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

[4]  Toshio Yanagida,et al.  Regulation of oxygen transport during brain activation: stimulus-induced hemodynamic responses in human and animal cortices , 2003, Dynamic medicine : DM.

[5]  Arthur W. Toga,et al.  Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex , 2004, The Journal of Neuroscience.

[6]  David A. Boas,et al.  Evidence that cerebral blood volume can provide brain activation maps with better spatial resolution than deoxygenated hemoglobin , 2005, NeuroImage.

[7]  Francisco Azuaje,et al.  BioMedical Engineering OnLine , 2005 .

[8]  A. Konstas,et al.  Neuroprotection for ischemic stroke using hypothermia , 2006, Neurocritical care.

[9]  T. Ishikawa,et al.  Local regulation of skin blood flow during cooling involving presynaptic P2 purinoceptors in rats , 2006, British journal of pharmacology.

[10]  Elizabeth M C Hillman,et al.  Optical brain imaging in vivo: techniques and applications from animal to man. , 2007, Journal of biomedical optics.

[11]  K. Rodenacker,et al.  Electrophysiologic assessment of sciatic nerve regeneration in the rat: Surrounding limb muscles feature strongly in recordings from the gastrocnemius muscle , 2007, Journal of Neuroscience Methods.

[12]  Lihong V. Wang,et al.  In vivo imaging of subcutaneous structures using functional photoacoustic microscopy , 2007, Nature Protocols.

[13]  Lihong V. Wang,et al.  Photoacoustic imaging of lacZ gene expression in vivo. , 2007, Journal of biomedical optics.

[14]  Lihong V. Wang,et al.  Biomedical Optics: Principles and Imaging , 2007 .

[15]  S. Morrison,et al.  A thermosensory pathway that controls body temperature , 2008, Nature Neuroscience.

[16]  Joshua E. Motelow,et al.  Negative BOLD with large increases in neuronal activity. , 2008, Cerebral cortex.

[17]  Ulrich Dirnagl,et al.  Hypothermia effects on neurovascular coupling and cerebral metabolic rate of oxygen , 2008, NeuroImage.

[18]  Manuchehr Soleimani,et al.  Medical imaging and physiological modelling: linking physics and biology , 2009, Biomedical engineering online.

[19]  A. Oraevsky,et al.  Laser optoacoustic imaging system for detection of breast cancer. , 2009, Journal of biomedical optics.

[20]  Jyh-Horng Chen,et al.  In vivo cerebromicrovasculatural visualization using 3D ΔR 2-based microscopy of magnetic resonance angiography (3DΔR 2-mMRA) , 2009, NeuroImage.

[21]  Lihong V. Wang,et al.  Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy. , 2009, Journal of biomedical optics.

[22]  Kartikeya Murari,et al.  High spatiotemporal resolution imaging of the neurovascular response to electrical stimulation of rat peripheral trigeminal nerve as revealed by in vivo temporal laser speckle contrast , 2009, Journal of Neuroscience Methods.

[23]  Nitish V. Thakor,et al.  Random process estimator for laser speckle imaging of cerebral blood flow , 2009, Optics express.

[24]  Nitish V. Thakor,et al.  High Resolution Cerebral Blood Flow Imaging by Registered Laser Speckle Contrast Analysis , 2010, IEEE Transactions on Biomedical Engineering.

[25]  Chin-Teng Lin,et al.  Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy , 2010, NeuroImage.

[26]  M. Cutolo,et al.  Capillaroscopy as an Outcome Measure for Clinical Trials on the Peripheral Vasculopathy in SSc—Is It Useful? , 2010, International journal of rheumatology.

[27]  Lihong V. Wang,et al.  Neurovascular Photoacoustic Tomography , 2010, Front. Neuroenerg..

[28]  S. Niehof,et al.  Neural influence on cold induced vasodilatation using a new set-up for bilateral measurement in the rat hind limb , 2010, Journal of Neuroscience Methods.

[29]  Afonso C. Silva,et al.  Spatiotemporal Evolution of the Functional Magnetic Resonance Imaging Response to Ultrashort Stimuli , 2011, The Journal of Neuroscience.

[30]  C. Willie,et al.  Cool head, hot brain: cerebral blood flow distribution during exercise , 2011, The Journal of physiology.

[31]  Neena K Sharma,et al.  The effect of exercise on neuropathic symptoms, nerve function, and cutaneous innervation in people with diabetic peripheral neuropathy. , 2012, Journal of diabetes and its complications.

[32]  C. Brennan,et al.  A Brain Tumor Molecular Imaging Strategy Using A New Triple-Modality MRI-Photoacoustic-Raman Nanoparticle , 2011, Nature Medicine.

[33]  Jyh-Yeong Chang,et al.  Transcranial Imaging of Functional Cerebral Hemodynamic Changes in Single Blood Vessels using in vivo Photoacoustic Microscopy , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  W. Tyler,et al.  Pulsed Ultrasound Differentially Stimulates Somatosensory Circuits in Humans as Indicated by EEG and fMRI , 2012, PloS one.

[35]  Lun-De Liao,et al.  Novel Trends in Biosensors Used for Electroencephalography Measurements in Neurocognitive Engineering Applications , 2012 .

[36]  Jyh-Yeong Chang,et al.  Investigation of the cerebral hemodynamic response function in single blood vessels by functional photoacoustic microscopy. , 2012, Journal of biomedical optics.

[37]  Fang Liu,et al.  Preliminary Evaluation of the Sural Nerve Using 22-MHz Ultrasound: A New Approach for Evaluation of Diabetic Cutaneous Neuropathy , 2012, PloS one.

[38]  S. Hovius,et al.  Thermoregulation in peripheral nerve injury-induced cold-intolerant rats. , 2012, Journal of plastic, reconstructive & aesthetic surgery : JPRAS.

[39]  Konstantin I Maslov,et al.  Living Brain Optical Imaging: Technology, Methods and Applications. , 2012, Journal of neuroscience and neuroengineering.

[40]  Harald Herkner,et al.  Hypothermia for neuroprotection in adults after cardiopulmonary resuscitation. , 2012, The Cochrane database of systematic reviews.

[41]  Stefano Taddei,et al.  Sympathetic regulation of vascular function in health and disease , 2012, Front. Physio..

[42]  S. Hovius,et al.  Cold-induced vasodilatation in cold-intolerant rats after nerve injury. , 2013, Journal of plastic, reconstructive & aesthetic surgery : JPRAS.

[43]  You-Yin Chen,et al.  Neurovascular coupling: in vivo optical techniques for functional brain imaging , 2013, BioMedical Engineering OnLine.

[44]  Yih-Kuen Jan,et al.  Skin blood flow response to locally applied mechanical and thermal stresses in the diabetic foot. , 2013, Microvascular research.