Brain surface temperature under a craniotomy.

Many neuroscientists access surface brain structures via a small cranial window, opened in the bone above the brain region of interest. Unfortunately this methodology has the potential to perturb the structure and function of the underlying brain tissue. One potential perturbation is heat loss from the brain surface, which may result in local dysregulation of brain temperature. Here, we demonstrate that heat loss is a significant problem in a cranial window preparation in common use for electrical recording and imaging studies in mice. In the absence of corrective measures, the exposed surface of the neocortex was at ∼28°C, ∼10°C below core body temperature, and a standing temperature gradient existed, with tissue below the core temperature even several millimeters into the brain. Cooling affected cellular and network function in neocortex and resulted principally from increased heat loss due to convection and radiation through the skull and cranial window. We demonstrate that constant perfusion of solution, warmed to 37°C, over the brain surface readily corrects the brain temperature, resulting in a stable temperature of 36-38°C at all depths. Our results indicate that temperature dysregulation may be common in cranial window preparations that are in widespread use in neuroscience, underlining the need to take measures to maintain the brain temperature in many physiology experiments.

[1]  L. Bindman,et al.  Comparison of the effects on electrocortical activity of general body cooling and local cooling of the surface of the brain , 1963 .

[2]  H. T. Hammel,et al.  CYCLIC VARIATIONS IN HYPOTHALAMIC TEMPERATURE IN UNANESTHETIZED RATS. , 1965, The American journal of physiology.

[3]  M. A. Baker,et al.  Role of cerebral arterial blood in the regulation of brain temperature in the monkey. , 1968, The American journal of physiology.

[4]  M. A. Baker,et al.  A comparative study of the role of the cerebral arterial blood in the regulation of brain temperature in five mammals. , 1969, Brain research.

[5]  M. A. Baker,et al.  Origin of temperature changes evoked in the brain by sensory stimulation. , 1973, Experimental neurology.

[6]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[7]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  P. Andersen,et al.  Association between brain temperature and dentate field potentials in exploring and swimming rats. , 1993, Science.

[9]  C. Wilson,et al.  Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. , 1994, Journal of neurophysiology.

[10]  F. Barone,et al.  Brain Cooling During Transient Focal Ischemia Provides Complete Neuroprotection , 1997, Neuroscience & Biobehavioral Reviews.

[11]  D. Kleinfeld,et al.  In vivo dendritic calcium dynamics in neocortical pyramidal neurons , 1997, Nature.

[12]  A. Larkman,et al.  The reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent , 1998, The Journal of physiology.

[13]  D. Ferster,et al.  Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex , 1999, Neuron.

[14]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[15]  T R Vidyasagar,et al.  Membrane properties and spike generation in rat visual cortical cells during reversible cooling , 2000, The Journal of physiology.

[16]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of rhythmic recurrent activity in neocortex , 2000, Nature Neuroscience.

[17]  Trichur Raman Vidyasagar,et al.  Synaptic transmission in the neocortex during reversible cooling , 2000, Neuroscience.

[18]  B. Sakmann,et al.  In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain , 2002, Pflügers Archiv.

[19]  J. Jack,et al.  Detailed passive cable models of layer 2/3 pyramidal cells in rat visual cortex at different temperatures , 2002, The Journal of physiology.

[20]  Winfried Denk,et al.  Targeted Whole-Cell Recordings in the Mammalian Brain In Vivo , 2003, Neuron.

[21]  A. Grinvald,et al.  Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Stosiek,et al.  In vivo two-photon calcium imaging of neuronal networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Bert Sakmann,et al.  Supralinear Ca2+ Influx into Dendritic Tufts of Layer 2/3 Neocortical Pyramidal Neurons In Vitro and In Vivo , 2003, The Journal of Neuroscience.

[24]  Charles J. Wilson,et al.  Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. , 2004, Journal of neurophysiology.

[25]  F. Helmchen,et al.  Boosting of Action Potential Backpropagation by Neocortical Network Activity In Vivo , 2004, The Journal of Neuroscience.

[26]  M. Volgushev,et al.  Probability of transmitter release at neocortical synapses at different temperatures. , 2004, Journal of neurophysiology.

[27]  Marc J. Assael,et al.  Thermal Conductivity of Polymethyl Methacrylate (PMMA) and Borosilicate Crown Glass BK7 , 2005 .

[28]  Dmitriy A Yablonskiy,et al.  How the body controls brain temperature: the temperature shielding effect of cerebral blood flow. , 2006, Journal of applied physiology.

[29]  Albert K. Lee,et al.  Whole-Cell Recordings in Freely Moving Rats , 2006, Neuron.

[30]  F. Helmchen,et al.  Background Synaptic Activity Is Sparse in Neocortex , 2006, The Journal of Neuroscience.

[31]  Srdjan D Antic,et al.  Voltage and calcium transients in basal dendrites of the rat prefrontal cortex , 2007, The Journal of physiology.

[32]  M. Fee,et al.  Using temperature to analyze temporal dynamics in the songbird motor pathway , 2008, Nature.

[33]  Tara A. Whitten,et al.  Heat synch: inter- and independence of body-temperature fluctuations and brain-state alternations in urethane-anesthetized rats. , 2009, Journal of neurophysiology.

[34]  Maria V. Sanchez-Vives,et al.  Temperature modulation of slow and fast cortical rhythms. , 2010, Journal of neurophysiology.

[35]  Spiking Patterns of Neocortical L5 Pyramidal Neurons in Vitro Change with Temperature , 2011, Front. Cell. Neurosci..

[36]  H. Gurden,et al.  Alteration of sensory-evoked metabolic and oscillatory activities in the olfactory bulb of GLAST-deficient mice , 2012, Front. Neural Circuits.

[37]  J. Ainge,et al.  Ontogeny of neural circuits underlying spatial memory in the rat , 2012, Front. Neural Circuits.

[38]  J. Waters,et al.  Effect of temperature on spiking patterns of neocortical layer 2/3 and layer 6 pyramidal neurons , 2012, Front. Neural Circuits.