Auditory thalamus bursts in anesthetized and non-anesthetized states: contribution to functional properties.

Over the last 10 years, high-frequency bursts of action potentials have been the subject of intense researches to understand their potential role in information encoding. Based on recordings from auditory thalamus neurons (n = 302) collected during anesthesia (pentobarbital, urethan, or ketamine/xylazine), waking (W), and slow-wave sleep (SWS), we investigated how bursts participate to frequency tuning, intensity-function, response latency (and latency variability), and stimulus detectability. Although present in all experimental conditions, bursts never dominated the cells mode of discharge: the highest proportion was found during ketamine/xylazine anesthesia (22%), the lowest during waking (4.5%). In all experimental conditions, bursts preferentially occurred at or around the cells best frequency (BF), thus increasing the frequency selectivity. This effect was observed at both the intensities producing the highest and the lowest evoked responses. Testing the intensity-functions indicated that for most of the cells, there was no systematic relationship between burst proportion and responses strength. Under several conditions (W, SWS, and urethan), when cells exhibited bursts >20%, the variability of their response latency was reduced in burst mode compared with single-spike mode. During W, this effect was accompanied by a reduction of the response latency. Finally, a receiver operating characteristic analysis indicated no particular relation between bursts and stimulus detectability. Compared with single-spike mode, which is present for broader frequency ranges, the prominence of bursts at the BF should contribute to filter information reaching the targets of medial geniculate cells at both cortical and subcortical levels.

[1]  S. Sherman,et al.  Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys , 2000, Visual Neuroscience.

[2]  John Eng,et al.  Receiver operating characteristic analysis: a primer. , 2005, Academic radiology.

[3]  W. Guido,et al.  Burst responses in thalamic relay cells of the awake behaving cat. , 1995, Journal of neurophysiology.

[4]  Muscarine induces an anomalous inhibition of synaptic transmission in rat auditory thalamic neurons in vitro. , 1995, The Journal of pharmacology and experimental therapeutics.

[5]  W. Guido,et al.  Burst and tonic response modes in thalamic neurons during sleep and wakefulness. , 2001, Journal of neurophysiology.

[6]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[7]  Fabrizio Gabbiani,et al.  Burst firing in sensory systems , 2004, Nature Reviews Neuroscience.

[8]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[9]  Jufang He,et al.  Differential distribution of burst and single-spike responses in auditory thalamus. , 2002, Journal of neurophysiology.

[10]  H. Swadlow,et al.  The impact of 'bursting' thalamic impulses at a neocortical synapse , 2001, Nature Neuroscience.

[11]  M. Steriade To burst, or rather, not to burst , 2001, Nature Neuroscience.

[12]  G Oakson,et al.  Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. , 1986, The Journal of physiology.

[13]  S. Sherman Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[14]  Alain Destexhe,et al.  The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  S. Sherman,et al.  Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. , 1992, Journal of neurophysiology.

[16]  J. Lisman Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[17]  H. Swadlow,et al.  Activation of a Cortical Column by a Thalamocortical Impulse , 2002, The Journal of Neuroscience.

[18]  Joseph E. LeDoux,et al.  LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit , 1995, Neuron.

[19]  R. Llinás,et al.  Electrophysiology of mammalian thalamic neurones in vitro , 1982, Nature.

[20]  E. Kaplan,et al.  Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. , 1995, Journal of neurophysiology.

[21]  E. Kvašňák,et al.  Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. , 1996, Audiology : official organ of the International Society of Audiology.

[22]  Ying-Shing Chan,et al.  An in vivo intracellular study of auditory thalamic neurons , 2003 .

[23]  S. Sherman,et al.  Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. , 1992, Journal of neurophysiology.

[24]  L. Maffei,et al.  Two firing patterns in the discharge of complex cells encoding different attributes of the visual stimulus , 2004, Experimental Brain Research.

[25]  V. Crunelli,et al.  A T‐type Ca2+ current underlies low‐threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. , 1989, The Journal of physiology.

[26]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[27]  I. Soltesz,et al.  Low‐frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. , 1991, The Journal of physiology.

[28]  M Steriade,et al.  Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Sherman,et al.  Response latencies of cells in the cat's lateral geniculate nucleus are less variable during burst than tonic firing , 1998, Visual Neuroscience.

[30]  F. de Ribaupierre,et al.  Corticofugal modulation of the information processing in the auditory thalamus of the cat , 2004, Experimental Brain Research.

[31]  G. Stuart,et al.  Action Potential Backpropagation and Somato-dendritic Distribution of Ion Channels in Thalamocortical Neurons , 2000, The Journal of Neuroscience.

[32]  Maxim Bazhenov,et al.  Short‐ and medium‐term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo , 2002, The Journal of physiology.

[33]  Jos J. Eggermont,et al.  Burst‐firing sharpens frequency‐tuning in primary auditory cortex , 1996, Neuroreport.

[34]  S. Murray Sherman,et al.  A wake-up call from the thalamus , 2001, Nature Neuroscience.

[35]  R. Llinás,et al.  Voltage-dependent burst-to-tonic switching of thalamic cell activity: an in vitro study. , 1984, Archives Italiennes de Biologie.

[36]  M. Ticku,et al.  An update on GABAA receptors , 1999, Brain Research Reviews.

[37]  D. McCormick,et al.  Functional implications of burst firing and single spike activity in lateral geniculate relay neurons , 1990, Neuroscience.

[38]  B. Hu,et al.  Lemniscal and non‐lemniscal synaptic transmission in rat auditory thalamus. , 1994, The Journal of physiology.

[39]  Frank C. Hoppensteadt,et al.  Bursts as a unit of neural information: selective communication via resonance , 2003, Trends in Neurosciences.

[40]  E. Puil,et al.  Pentobarbital depressant effects are independent of GABA receptors in auditory thalamic neurons. , 2002, Journal of neurophysiology.

[41]  B. Hu Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. , 1995, The Journal of physiology.

[42]  E. Evans Neuroleptanesthesia for the guinea pig. An ideal anesthetic procedure for long-term physiological studies of the cochlea. , 1979, Archives of otolaryngology.

[43]  A. Destexhe,et al.  Dendritic Low-Threshold Calcium Currents in Thalamic Relay Cells , 1998, The Journal of Neuroscience.

[44]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[45]  R. Nicoll,et al.  General anesthetics hyperpolarize neurons in the vertebrate central nervous system. , 1982, Science.

[46]  G. Barrionuevo,et al.  Lateral geniculate nucleus unitary discharge in sleep and waking: state- and rate-specific aspects. , 1983, Journal of neurophysiology.

[47]  J. Hirsch,et al.  Sleep-related variations of membrane potential in the lateral geniculate body relay neurons of the cat , 1983, Brain Research.

[48]  Edward L. Bartlett,et al.  Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. , 1999, Journal of neurophysiology.

[49]  M. Pirchio,et al.  Postnatal Development of Membrane Properties and δ Oscillations in Thalamocortical Neurons of the Cat Dorsal Lateral Geniculate Nucleus , 1997, The Journal of Neuroscience.

[50]  J. Edeline,et al.  Auditory thalamus neurons during sleep: changes in frequency selectivity, threshold, and receptive field size. , 2000, Journal of neurophysiology.

[51]  E. Puil,et al.  Mechanisms for signal transformation in lemniscal auditory thalamus. , 1996, Journal of neurophysiology.

[52]  Joseph E LeDoux,et al.  Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[54]  E. Kvašňák,et al.  Discharge properties of neurons in subdivisions of the medial geniculate body of the guinea pig. , 2000, Physiological research.

[55]  F. de Ribaupierre,et al.  Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions , 1994, Neuroscience Research.

[56]  D. McCormick,et al.  Actions of acetylcholine in the guinea‐pig and cat medial and lateral geniculate nuclei, in vitro. , 1987, The Journal of physiology.

[57]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

[59]  D. Hubel,et al.  The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[61]  T E Cohn,et al.  Receiver operating characteristic analysis. Application to the study of quantum fluctuation effects in optic nerve of Rana pipiens , 1975, The Journal of general physiology.

[62]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Jean-Marc Edeline,et al.  Bursts in the medial geniculate body: a comparison between anesthetized and unanesthetized states in guinea pig , 2003, Experimental Brain Research.

[64]  S. Sherman,et al.  Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode , 1995, Visual Neuroscience.