Dynamics of infraslow potentials in the primary auditory cortex: Component analysis and contribution of specific thalamic-cortical and non-specific brainstem–cortical influences

Several available reports demonstrate the presence of infraslow activity (<0.5 Hz) in structures of the auditory system of the brain. It was reported earlier that specific alterations of this activity in the domain of seconds (0.1-0.5 Hz) occurred in the medial geniculate nucleus (MGN) and primary auditory cortex (A1) in response to acoustic stimuli. The present study was performed to test two hypotheses: (1) that potentials in the domain of seconds (0.1-0.5 Hz) reflect specific and direct interactions of the MGN and A1 during neural processing of sensory information, and (2) that low-frequency infraslow potentials in the A1 (<0.1 Hz) are related to brainstem influences originating from the locus coeruleus (LC) and dorsal raphe nucleus (DRN). The experimental subjects were 25 adult rats with chronic stereotaxic electrodes implanted in the MGN, A1, LC, and DRN. The animals were anesthetized and infraslow activity was once recorded under several experimental conditions: (1) in the A1 before and after electrical stimulation of MGN, (2) in the A1 before and after electrical stimulation of LC, and (3) in the A1 before and after electrical stimulation of DRN. The effects of MGN stimulation were limited to overall increases in spectral power in the frequency domain of 0.1-0.5 Hz. Specifically, power increased in the frequencies of 0.1-0.25, 0.35-0.4, and 0.45-0.5 Hz in the A1 after MGN stimulation. The electrical stimulation of either the LC or DRN affected only multisecond activity (0.0167-0.04 Hz) in the A1 in the similar way (increase of powers of multisecond potentials), but it does not induced any changes in the activity with the frequencies of 0.1-0.5 Hz in this structure. These results support tentative conclusions that infraslow activity in the range of 0.1-0.5 Hz is implicated in specific mechanisms of interactions within the MGN-A1 thalamic-cortical system, whereas multisecond potentials (0.0167-0.04 Hz) in A1 are mainly attributed to the influences of brainstem nuclei (like LC and DRN) on general neuronal excitability of this auditory cortical area.

[1]  I. G. Sil’kis Excitatory interactions in neuronal networks which include cells of the auditory cortex and the medial geniculate body , 1995, Neuroscience and Behavioral Physiology.

[2]  H. J. Crow,et al.  Toxic effects of intra-cerebral electrodes , 1966, Medical and biological engineering.

[3]  R. Llinás,et al.  Bursting of thalamic neurons and states of vigilance. , 2006, Journal of neurophysiology.

[4]  Valéria Csépe,et al.  Auditory Evoked Potentials Reflect Serotonergic Neuronal Activity—A Study in Behaving Cats Administered Drugs Acting on 5-HT1A Autoreceptors in the Dorsal Raphe Nucleus , 1999, Neuropsychopharmacology.

[5]  J. Voipio,et al.  Full-band EEG (FbEEG): an emerging standard in electroencephalography , 2005, Clinical Neurophysiology.

[6]  H. Scheich,et al.  Stimulus-related gamma oscillations in primate auditory cortex. , 2002, Journal of neurophysiology.

[7]  H. Hurst,et al.  Measurement of ethyl carbamate in blood by capillary gas chromatography/mass spectrometry using selected ion monitoring. , 1990, Biomedical & environmental mass spectrometry.

[8]  M. Zimmermann,et al.  Demonstration of extensive brainstem projections to medial and lateral thalamus and hypothalamus in the rat , 1990, Neuroscience.

[9]  Wolf Singer,et al.  Features of neuronal synchrony in mouse visual cortex. , 2003, Journal of neurophysiology.

[10]  M. Schönwiesner,et al.  Hemispheric asymmetry for auditory processing in the human auditory brain stem, thalamus, and cortex. , 2006, Cerebral cortex.

[11]  S. S. Fox,et al.  Localization and habituation of sensory evoked dc responses in cat cortex. , 1966, Experimental neurology.

[12]  E Ahissar,et al.  Possible involvement of neuromodulatory systems in cortical Hebbian-like plasticity , 1996, Journal of Physiology-Paris.

[13]  A. Robles,et al.  N1/P2 component of auditory evoked potential reflect changes of the brain serotonin biosynthesis in rats , 2005, Nutritional neuroscience.

[14]  Steven B. Lowen,et al.  Emotional task-dependent low-frequency fluctuations and methylphenidate: Wavelet scaling analysis of 1/f-type fluctuations in fMRI of the cerebellar vermis , 2006, Journal of Neuroscience Methods.

[15]  M. Teich,et al.  Fractal character of the neural spike train in the visual system of the cat. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[16]  G. Juckel,et al.  Serotonergic effects of smoking are independent from the human serotonin transporter gene promoter polymorphism: evidence from auditory cortical stimulus processing. , 2005, Pharmacopsychiatry.

[17]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[18]  S. Hellström,et al.  Specific sound-induced noradrenergic and serotonergic activation in central auditory structures , 1998, Hearing Research.

[19]  Pat Levitt,et al.  Noradrenaline neuron innervation of the neocortex in the rat , 1978, Brain Research.

[20]  J. Winer,et al.  Origins of medial geniculate body projections to physiologically defined zones of rat primary auditory cortex , 1999, Hearing Research.

[21]  M. Steriade Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[22]  H Shibasaki,et al.  Reappraisal of the effect of electrode property on recording slow potentials. , 1998, Electroencephalography and clinical neurophysiology.

[23]  Larry W. Swanson,et al.  Brain Maps: Structure of the Rat Brain , 1992 .

[24]  R. Metherate,et al.  Auditory thalamocortical transmission is reliable and temporally precise. , 2005, Journal of neurophysiology.

[25]  L. Sokoloff,et al.  The central noradrenergic system in the rat: Metabolic mapping with α-adrenergic blocking agents , 1982, Brain Research.

[26]  P. Tallgren,et al.  Evaluation of commercially available electrodes and gels for recording of slow EEG potentials , 2005, Clinical Neurophysiology.

[27]  E. Rouiller,et al.  Extrathalamic ascending projections to physiologically identified fields of the cat auditory cortex , 1989, Hearing Research.

[28]  T. Yuen,et al.  Tissue response to potential neuroprosthetic materials implanted subdurally. , 1987, Biomaterials.

[29]  Igor V. Filippov,et al.  Sound-induced changes of infraslow brain potential fluctuations in the medial geniculate nucleus and primary auditory cortex in anaesthetized rats , 2007, Brain Research.

[30]  S. Goldring,et al.  D-C POTENTIALS OF THE BRAIN. , 1964, Physiological reviews.

[31]  W F Jackson,et al.  Toxic Effects of Silver‐Silver Chloride Electrodes on Vascular Smooth Muscle , 1983, Circulation research.

[32]  Mitchell Steinschneider,et al.  Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. , 2008, Cerebral cortex.

[33]  Igor V. Filippov,et al.  Very slow potentials in the lateral geniculate complex and primary visual cortex during different illumination changes in freely moving rats , 2004, Neuroscience Letters.

[34]  I. V. Filippov Very slow brain potential fluctuations (< 0.5 Hz) in visual thalamus and striate cortex after their successive electrical stimulation in lightly anesthetized rats , 2005, Brain Research.

[35]  N. A. ALADJALOVA,et al.  Infra-Slow Rhythmic Oscillations of The Steady Potential of the Cerebral Cortex , 1957, Nature.

[36]  Y. Ogawa Firing properties of olfactory bulb neurons during sniffing in rats , 1998, Physiology & Behavior.

[37]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[38]  P. Fadel,et al.  Fractal properties of human muscle sympathetic nerve activity. , 2004, American journal of physiology. Heart and circulatory physiology.

[39]  V. Frolov,et al.  Very slow potential oscillations in locus coeruleus and dorsal raphe nucleus under different illumination in freely moving rats , 2004, Neuroscience Letters.

[40]  P. Larsen,et al.  Long-term correlations in the spike trains of medullary sympathetic neurons. , 2001, Journal of neurophysiology.

[41]  I. V. Filippov Power spectral analysis of very slow brain potential oscillations in primary visual cortex of freely moving rats during darkness and light , 2003, Neurocomputing.

[42]  P. Finkenzeller,et al.  Akustischen Reizen zugeordnete Gleichspannungsänderungen am intakten Schädel des Menschen , 2004, Pflügers Archiv.

[43]  Suzanne S. Stensaas,et al.  Histopathological evaluation of materials implanted in the cerebral cortex , 1978, Acta Neuropathologica.

[44]  D. Su,et al.  Asynchronism of the Recovery of Baroreflex Sensitivity, Blood Pressure, and Consciousness from Anesthesia in Rats , 2004, Journal of cardiovascular pharmacology.

[45]  C. Harley Norepinephrine and Dopamine as Learning Signals , 2004, Neural plasticity.

[46]  M. Steriade Impact of network activities on neuronal properties in corticothalamic systems. , 2001, Journal of neurophysiology.

[47]  Theodore H Bullock Slow potentials in the brain: still little understood but gradually getting analytical attention , 1999, Brain Research Bulletin.

[48]  Pablo Fuentealba,et al.  Synaptic plasticity in local cortical network in vivo and its modulation by the level of neuronal activity. , 2006, Cerebral cortex.

[49]  I. Ebenezer The generation of cortical slow potentials in the rat anaesthetised with urethane and their modification by nicotine , 1986, Neuropharmacology.

[50]  W. Keidel,et al.  Reizkorrelierte Gleichspannungsänderungen der primären Hörrinde an der wachen Katze , 1969, Pflügers Archiv.

[51]  S. Cruikshank,et al.  Auditory thalamocortical synaptic transmission in vitro. , 2002, Journal of neurophysiology.

[52]  Jufang He,et al.  Slow Oscillation in Non-Lemniscal Auditory Thalamus , 2003, The Journal of Neuroscience.

[53]  Igor V. Filippov,et al.  Role of infraslow (0-0.5 Hz) potential oscillations in the regulation of brain stress response by the locus coeruleus system , 2002, Neurocomputing.

[54]  R. Gumnit D.C. potential changes from auditory cortex of cat. , 1960, Journal of neurophysiology.

[55]  P. Novak,et al.  Slow modulation of EEG , 1992, Neuroreport.

[56]  W D Keidel,et al.  [Sound correlated d-c changes from the intact head of human subjects]. , 1969, Pflugers Archiv : European journal of physiology.

[57]  E. Basar The theory of the whole-brain-work. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  Jyrki Ahveninen,et al.  Serotonin Modulates Early Cortical Auditory Processing in Healthy Subjects. Evidence from MEG with Acute Tryptophan Depletion , 2002, Neuropsychopharmacology.

[59]  M. Steriade Corticothalamic resonance, states of vigilance and mentation , 2000, Neuroscience.

[60]  J. Schnupp,et al.  Tuning to Natural Stimulus Dynamics in Primary Auditory Cortex , 2006, Current Biology.

[61]  B. Hu,et al.  Burst firing induces a slow after hyperpolarization in rat auditory thalamus , 2005, Neuroscience Letters.

[62]  J. Edeline,et al.  Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. , 2004, Journal of neurophysiology.

[63]  M. Berry,et al.  The response of the cerebral hemisphere of the rat to injury. II. The neonatal rat. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.