Auditory cortex of the marmoset monkey – complex responses to tones and vocalizations under opiate anaesthesia in core and belt areas

Many anaesthetics commonly used in auditory research severely depress cortical responses, particularly in the supragranular layers of the primary auditory cortex and in non‐primary areas. This is particularly true when stimuli other than simple tones are presented. Although awake preparations allow better preservation of the neuronal responses, there is an inherent limitation to this approach whenever the physiological data need to be combined with histological reconstruction or anatomical tracing. Here we tested the efficacy of an opiate‐based anaesthetic regime to study physiological responses in the primary auditory cortex and middle lateral belt area. Adult marmosets were anaesthetized using a combination of sufentanil (8 μg/kg/h, i.v.) and N2O (70%). Unit activity was recorded throughout the cortical layers, in response to auditory stimuli presented binaurally. Stimuli consisted of a battery of tones presented at different intensities, as well as two marmoset calls (‘Tsik’ and ‘Twitter’). In addition to robust monotonic and non‐monotonic responses to tones, we found that the neuronal activity reflected various aspects of the calls, including ‘on’ and ‘off’ components, and temporal fluctuations. Both phasic and tonic activities, as well as excitatory and inhibitory components, were observed. Furthermore, a late component (100–250 ms post‐offset) was apparent. Our results indicate that the sufentanil/N2O combination allows better preservation of response patterns in both the core and belt auditory cortex, in comparison with anaesthetics usually employed in auditory physiology. This anaesthetic regime holds promise in enabling the physiological study of complex auditory responses in acute preparations, combined with detailed anatomical and histological investigation.

[1]  Michael Petrides,et al.  The marmoset brain in stereotaxic coordinates , 2012 .

[2]  Leo L. Lui,et al.  Functional response properties of neurons in the dorsomedial visual area of New World monkeys (Callithrix jacchus). , 2006, Cerebral cortex.

[3]  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.

[4]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[5]  C. Galletti,et al.  Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex , 2009, The Journal of Neuroscience.

[6]  Kerry M. M. Walker,et al.  Linking Cortical Spike Pattern Codes to Auditory Perception , 2008, Journal of Cognitive Neuroscience.

[7]  R Gattass,et al.  Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and old World monkeys , 1993, Visual Neuroscience.

[8]  J. Miller,et al.  Response pattern complexity of auditory cells in the cortex of unanesthetized monkeys. , 1974, Brain research.

[9]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Joachim Ostwald,et al.  Complexity and temporal dynamics of frequency coding in the awake rat auditory cortex , 2003, The European journal of neuroscience.

[11]  Guangying K. Wu,et al.  Defining cortical frequency tuning with recurrent excitatory circuitry , 2007, Nature Neuroscience.

[12]  Lisa A. de la Mothe,et al.  A comparison of neuron response properties in areas A1 and CM of the marmoset monkey auditory cortex: tones and broadband noise. , 2005, Journal of neurophysiology.

[13]  S. Yin,et al.  Cortical responses to amplitude modulation in guinea pigs and the effects of general anesthesia by pentobarbital , 2009, Hearing Research.

[14]  T. Stanley,et al.  Comparison of sufentanil-oxygen and fentanyl-oxygen anesthesia for mitral and aortic valvular surgery. , 1988, Journal of cardiothoracic anesthesia.

[15]  Matthew W Spitzer,et al.  Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing , 2009, The European journal of neuroscience.

[16]  C. Atencio,et al.  Frequency-modulation encoding in the primary auditory cortex of the awake owl monkey. , 2007, Journal of neurophysiology.

[17]  T. Kitama,et al.  Time course of tonal frequency-response-area of primary auditory cortex neurons in alert cats , 2003, Neuroscience Research.

[18]  D. P. Phillips,et al.  Central auditory onset responses, and temporal asymmetries in auditory perception , 2002, Hearing Research.

[19]  D. P. Phillips,et al.  Response timing constraints on the cortical representation of sound time structure. , 1990, The Journal of the Acoustical Society of America.

[20]  R. Rajan Centrifugal Pathways Protect Hearing Sensitivity at the Cochlea in Noisy Environments That Exacerbate the Damage Induced by Loud Sound , 2000, The Journal of Neuroscience.

[21]  J N Lunn,et al.  Monitoring in anaesthesia. , 1970, Biomedical engineering.

[22]  Srivatsun Sadagopan,et al.  Nonlinear Spectrotemporal Interactions Underlying Selectivity for Complex Sounds in Auditory Cortex , 2009, The Journal of Neuroscience.

[23]  G. Recanzone,et al.  Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. , 2000, Journal of neurophysiology.

[24]  A. R. Palmer,et al.  Laminar differences in the response properties of cells in the primary auditory cortex , 2007, Experimental Brain Research.

[25]  Xiaoqin Wang,et al.  Level Invariant Representation of Sounds by Populations of Neurons in Primary Auditory Cortex , 2008, The Journal of Neuroscience.

[26]  C. Schreiner,et al.  Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. , 2003, Cerebral cortex.

[27]  R. Klinke,et al.  Monitoring of anaesthesia in neurophysiological experiments. , 1999, Neuroreport.

[28]  V. Mountcastle,et al.  Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli. , 1957, Journal of neurophysiology.

[29]  C. Atencio,et al.  Laminar diversity of dynamic sound processing in cat primary auditory cortex. , 2010, Journal of neurophysiology.

[30]  W. Sadee,et al.  Opiate receptor binding-effect relationship: Sufentanil and etorphine produce analgesia at the μ-site with low fractional receptor occupancy , 1984, Brain Research.

[31]  M. Kilgard,et al.  Anesthesia suppresses nonsynchronous responses to repetitive broadband stimuli , 2007, Neuroscience.

[32]  I. Nelken,et al.  Responses of Neurons in Cat Primary Auditory Cortex to Bird Chirps: Effects of Temporal and Spectral Context , 2002, The Journal of Neuroscience.

[33]  Xiaoqin Wang,et al.  Contribution of Inhibition to Stimulus Selectivity in Primary Auditory Cortex of Awake Primates , 2010, The Journal of Neuroscience.

[34]  Josef Syka,et al.  Responses to species-specific vocalizations in the auditory cortex of awake and anesthetized guinea pigs , 2005, Hearing Research.

[35]  Hisayuki Ojima,et al.  Interplay of excitation and inhibition elicited by tonal stimulation in pyramidal neurons of primary auditory cortex , 2011, Neuroscience & Biobehavioral Reviews.

[36]  R. Rajan,et al.  Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity , 1998, Nature Neuroscience.

[37]  J. Ostwald,et al.  Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. , 2001, Journal of neurophysiology.

[38]  M. DeWeese,et al.  Binary Spiking in Auditory Cortex , 2003, The Journal of Neuroscience.

[39]  Jan W. H. Schnupp,et al.  Plasticity of Temporal Pattern Codes for Vocalization Stimuli in Primary Auditory Cortex , 2006, The Journal of Neuroscience.

[40]  M. Gamberini,et al.  Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[41]  Suppression of auditory cortical activities in awake cats by pure tone stimuli , 2004, Neuroscience Letters.

[42]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[43]  M. Wehr,et al.  Nonoverlapping Sets of Synapses Drive On Responses and Off Responses in Auditory Cortex , 2010, Neuron.

[44]  Biao Tian,et al.  Processing of frequency-modulated sounds in the lateral auditory belt cortex of the rhesus monkey. , 2004, Journal of neurophysiology.

[45]  S. Lomber,et al.  Evidence for Hierarchical Processing in Cat Auditory Cortex: Nonreciprocal Influence of Primary Auditory Cortex on the Posterior Auditory Field , 2009, The Journal of Neuroscience.

[46]  H. Funkenstein,et al.  Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys , 1973, Experimental Brain Research.

[47]  P. Lennie,et al.  Chromatic mechanisms in striate cortex of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  Jean-Marc Edeline,et al.  A Spike-Timing Code for Discriminating Conspecific Vocalizations in the Thalamocortical System of Anesthetized and Awake Guinea Pigs , 2009, The Journal of Neuroscience.

[49]  I. Volkov,et al.  Formation of spike response to sound tones in cat auditory cortex neurons: Interaction of excitatory and inhibitory effects , 1991, Neuroscience.

[50]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[51]  C. Schreiner,et al.  Auditory cortical neuron response differences under isoflurane versus pentobarbital anesthesia , 2001, Hearing Research.

[52]  Marcello G P Rosa,et al.  Preparation for the in vivo recording of neuronal responses in the visual cortex of anaesthetised marmosets (Callithrix jacchus). , 2003, Brain research. Brain research protocols.

[53]  D. Bendor,et al.  Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys. , 2008, Journal of neurophysiology.

[54]  Yu Sato,et al.  Heterogeneous neuronal responses to frequency-modulated tones in the primary auditory cortex of awake cats. , 2008, Journal of neurophysiology.

[55]  Tristan A. Chaplin,et al.  A Specialized Area in Limbic Cortex for Fast Analysis of Peripheral Vision , 2012, Current Biology.

[56]  M. Sutter Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. , 2000, Journal of neurophysiology.

[57]  N. Pace,et al.  Comparison of Sufentanil–N2O and Fentanyl–N2O in Patients Without Cardiac Disease Undergoing General Surgery , 1987, Anesthesiology.

[58]  Michael B. Calford,et al.  Monaural inhibition in cat auditory cortex. , 1995, Journal of neurophysiology.

[59]  I. Nelken,et al.  Responses to linear and logarithmic frequency‐modulated sweeps in ferret primary auditory cortex , 2000, The European journal of neuroscience.

[60]  Lindsay Aitkin,et al.  Audition and the auditory pathway of a vocal new world primate, the common marmoset , 1993, Progress in Neurobiology.

[61]  Xiaoqin Wang,et al.  Sustained firing in auditory cortex evoked by preferred stimuli , 2005, Nature.

[62]  M. Todd,et al.  Anesthesia for craniotomy: a double-blind comparison of alfentanil, fentanyl, and sufentanil. , 1990, Anesthesiology.

[63]  Xiaoqin Wang,et al.  Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. , 2003, Journal of neurophysiology.

[64]  Matthew W Spitzer,et al.  Anatomical and physiological definition of the motor cortex of the marmoset monkey , 2008, The Journal of comparative neurology.

[65]  Yoshinao Kajikawa,et al.  Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[66]  S H Snyder,et al.  The opiate receptor. , 1975, Neurosciences Research Program bulletin.

[67]  C. Schreiner,et al.  Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. , 2002, Journal of neurophysiology.

[68]  S. Yin,et al.  General anesthesia changes gap-evoked auditory responses in guinea pigs , 2007, Acta oto-laryngologica.

[69]  Ewan A. Macpherson,et al.  Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex , 2008, Hearing Research.

[70]  Xiaoqin Wang,et al.  Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. , 2001, Journal of neurophysiology.

[71]  P. Jen,et al.  Interaction between excitation and inhibition affects frequency tuning curve, response size and latency of neurons in the auditory cortex of the big brown bat, Eptesicus fuscus , 2002, Hearing Research.

[72]  J. Waters,et al.  Brain surface temperature under a craniotomy. , 2012, Journal of neurophysiology.

[73]  Christophe Jouffrais,et al.  Single-unit responses in the auditory cortex of monkeys performing a conditional acousticomotor task , 2003, Experimental Brain Research.

[74]  Robert A. A. Campbell,et al.  Brief Sounds Evoke Prolonged Responses in Anesthetized Ferret Auditory Cortex , 2010, Journal of neurophysiology.

[75]  I. Nelken,et al.  Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. , 2006, Journal of neurophysiology.

[76]  G. Epple,et al.  Comparative studies on vocalization in marmoset monkeys (Hapalidae). , 1968, Folia primatologica; international journal of primatology.

[77]  E. G. Jones,et al.  Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys , 1997, The Journal of comparative neurology.

[78]  G. Gerstein,et al.  Trial-to-Trial Variability and State-Dependent Modulation of Auditory-Evoked Responses in Cortex , 1999, The Journal of Neuroscience.

[79]  G. Plourde,et al.  The long-latency auditory evoked potential as a measure of the level of consciousness during sufentanil anesthesia. , 1991, Journal of cardiothoracic and vascular anesthesia.

[80]  J. Leysen,et al.  [3H]Sufentanil, a superior ligand for mu-opiate receptors: binding properties and regional distribution in rat brain and spinal cord. , 1983, European journal of pharmacology.

[81]  M. Merzenich,et al.  Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus) , 1986, The Journal of comparative neurology.

[82]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[83]  D. P. Phillips Temporal response features of cat auditory cortex neurons contributing to sensitivity to tones delivered in the presence of continuous noise , 1985, Hearing Research.

[84]  Z. Wollberg,et al.  Tuning properties of auditory cortex cells in the awake squirrel monkey , 2004, Experimental Brain Research.

[85]  Yu Sato,et al.  Differential representation of spectral and temporal information by primary auditory cortex neurons in awake cats: Relevance to auditory scene analysis , 2009, Brain Research.

[86]  A. R. Palmer,et al.  Location of cells giving phase-locked responses to pure tones in the primary auditory cortex , 2011, Hearing Research.

[87]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[88]  J. Newman,et al.  Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. , 1973, Brain research.

[89]  Anthony G. Hudetz,et al.  Suppressing consciousness: Mechanisms of general anesthesia , 2006 .

[90]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.