Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI

Much of what is known about the cortical organization for audition in humans draws from studies of auditory cortex in the cat. However, these data build largely on electrophysiological recordings that are both highly invasive and provide less evidence concerning macroscopic patterns of brain activation. Optical imaging, using intrinsic signals or dyes, allows visualization of surface-based activity but is also quite invasive. Functional magnetic resonance imaging (fMRI) overcomes these limitations by providing a large-scale perspective of distributed activity across the brain in a non-invasive manner. The present study used fMRI to characterize stimulus-evoked activity in auditory cortex of an anesthetized (ketamine/isoflurane) cat, focusing specifically on the blood-oxygen-level-dependent (BOLD) signal time course. Functional images were acquired for adult cats in a 7 T MRI scanner. To determine the BOLD signal time course, we presented 1s broadband noise bursts between widely spaced scan acquisitions at randomized delays (1-12 s in 1s increments) prior to each scan. Baseline trials in which no stimulus was presented were also acquired. Our results indicate that the BOLD response peaks at about 3.5s in primary auditory cortex (AI) and at about 4.5 s in non-primary areas (AII, PAF) of cat auditory cortex. The observed peak latency is within the range reported for humans and non-human primates (3-4 s). The time course of hemodynamic activity in cat auditory cortex also occurs on a comparatively shorter scale than in cat visual cortex. The results of this study will provide a foundation for future auditory fMRI studies in the cat to incorporate these hemodynamic response properties into appropriate analyses of cat auditory cortex.

[1]  Aysenil Belger,et al.  Hemodynamic correlates of stimulus repetition in the visual and auditory cortices: an fMRI study , 2004, NeuroImage.

[2]  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.

[3]  J. Rauschecker.  Cortical processing of complex sounds , 1998, Current Opinion in Neurobiology.

[4]  J. Eggermont,et al.  Increasing Spectrotemporal Sound Density Reveals an Octave-Based Organization in Cat Primary Auditory Cortex , 2008, The Journal of Neuroscience.

[5]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[6]  G. Mangun,et al.  Tonotopy in human auditory cortex examined with functional magnetic resonance imaging , 1997, Human brain mapping.

[7]  Tao Jin,et al.  Isoflurane anesthesia effect in functional imaging studies , 2007, NeuroImage.

[8]  J. Eggermont,et al.  Long-term, partially-reversible reorganization of frequency tuning in mature cat primary auditory cortex can be induced by passive exposure to moderate-level sounds , 2009, Hearing Research.

[9]  P. van Dijk,et al.  Simultaneous sampling of event‐related BOLD responses in auditory cortex and brainstem , 2002, Magnetic resonance in medicine.

[10]  C E Schreiner,et al.  Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. I. Intensity dependence of firing rate and response latency. , 1994, Journal of neurophysiology.

[11]  J. Weeks,et al.  Comparative effects of propofol, pentobarbital, and isoflurane on cerebral blood flow and blood volume. , 1996, Journal of neurosurgical anesthesiology.

[12]  N. Logothetis,et al.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex , 2006, PLoS biology.

[13]  J. Meyer,et al.  Neurogenic control of cerebral blood flow in the baboon. , 1975, Journal of neurosurgery.

[14]  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.

[15]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[16]  Dae-Shik Kim,et al.  High-resolution mapping of iso-orientation columns by fMRI , 2000, Nature Neuroscience.

[17]  Stefan A. Carp,et al.  The effect of different anesthetics on neurovascular coupling , 2010, NeuroImage.

[18]  A. Toga,et al.  5 – Optical Imaging Based on Intrinsic Signals , 2002 .

[19]  Donald S. Williams,et al.  Cerebral perfusion during anesthesia with fentanyl, isoflurane, or pentobarbital in normal rats studied by arterial spin‐labeled MRI , 2001, Magnetic resonance in medicine.

[20]  Peter Jezzard,et al.  An in vivo model for functional MRI in cat visual cortex , 1997, Magnetic resonance in medicine.

[21]  W. Muir,et al.  Handbook of Veterinary Anesthesia , 2000 .

[22]  Stephen G. Lomber,et al.  Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32 , 2010, Hearing Research.

[23]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Rouiller,et al.  Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas , 2004, Experimental Brain Research.

[25]  Hans-Jochen Heinze,et al.  A movement-sensitive area in auditory cortex , 1999, Nature.

[26]  Stephen G Lomber,et al.  Reciprocal Modulatory Influences between Tonotopic and Nontonotopic Cortical Fields in the Cat , 2010, The Journal of Neuroscience.

[28]  Zhang Kun,et al.  PROGRESS IN VISUAL CORTICAL RESEARCH USING OPTICAL IMAGING BASED ON INTRINSIC SIGNALS , 2000 .

[29]  The Auditory Cortex , 1982 .

[30]  Ben Godde,et al.  Optical Imaging of Cat Auditory Cortex Cochleotopic Selectivity Evoked by Acute Electrical Stimulation of a Multi‐channel Cochlear Implant , 1997, The European journal of neuroscience.

[31]  J. Pettigrew,et al.  Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat. , 2001, Journal of neurophysiology.

[32]  A. Crane,et al.  Local Changes in Cerebral Glucose Utilization during Ketamine Anesthesia , 1982, Anesthesiology.

[33]  P. Knight,et al.  Representation of the cochlea within the anterior auditory field (AAF) of the cat , 1977, Brain Research.

[34]  Dave R. M. Langers,et al.  Lateralization, connectivity and plasticity in the human central auditory system , 2005, NeuroImage.

[35]  Charles C Lee,et al.  Convergence of thalamic and cortical pathways in cat auditory cortex , 2011, Hearing Research.

[36]  S. Lomber,et al.  Neuronal activation times to simple, complex, and natural sounds in cat primary and nonprimary auditory cortex. , 2011, Journal of neurophysiology.

[37]  S. Lomber,et al.  Differential Modulatory Influences between Primary Auditory Cortex and the Anterior Auditory Field , 2009, The Journal of Neuroscience.

[38]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[39]  L Martyn Klassen,et al.  Robust automated shimming technique using arbitrary mapping acquisition parameters (RASTAMAP) , 2004, Magnetic resonance in medicine.

[40]  Dae-Shik Kim,et al.  Origin of Negative Blood Oxygenation Level—Dependent fMRI Signals , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  M. L. Sutter,et al.  Functional topography of cat primary auditory cortex: response latencies , 1997, Journal of Comparative Physiology A.

[42]  Alan C. Evans,et al.  Event-Related fMRI of the Auditory Cortex , 1998, NeuroImage.

[43]  Kamil Ugurbil,et al.  Retinotopic mapping in cat visual cortex using high-field functional magnetic resonance imaging , 2003, Journal of Neuroscience Methods.

[44]  H. Ojima,et al.  Isofrequency band-like zones of activation revealed by optical imaging of intrinsic signals in the cat primary auditory cortex. , 2005, Cerebral cortex.

[45]  D. Irvine,et al.  Functional specialization in auditory cortex: responses to frequency-modulated stimuli in the cat's posterior auditory field. , 1998, Journal of neurophysiology.

[46]  O. Scremin,et al.  Cholinergic Control of Blood Flow in the Cerebral Cortex of the Rat , 1973, Stroke.

[47]  Li Sun,et al.  Newcastle University E-prints Citation for Published Item: Further Information on Publisher Website: Publishers Copyright Statement: Use Policy: Characterisation of the Bold Response Time Course at Different Levels of the Auditory Pathway in Non-human Primates , 2022 .

[48]  A. Dale,et al.  Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. , 2004, Journal of neurophysiology.

[49]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[50]  K. Scheffler,et al.  Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI , 1998, Hearing Research.

[51]  Robert V. Harrison,et al.  Three Distinct Auditory Areas of Cortex (AI, AII, and AAF) Defined by Optical Imaging of Intrinsic Signals , 2000, NeuroImage.

[52]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[53]  S. Lomber,et al.  Double dissociation of 'what' and 'where' processing in auditory cortex , 2008, Nature Neuroscience.

[54]  H. Dinse,et al.  The timing of processing along the visual pathway in the cat. , 1994, Neuroreport.

[55]  Charles C Lee,et al.  Connections of cat auditory cortex: III. Corticocortical system , 2008, The Journal of comparative neurology.

[56]  Nikos K Logothetis,et al.  Optimizing the imaging of the monkey auditory cortex: sparse vs. continuous fMRI. , 2009, Magnetic resonance imaging.

[57]  Lee M. Miller,et al.  Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. , 2002, Journal of neurophysiology.