Mouse auditory cortex differs from visual and somatosensory cortices in the laminar distribution of cytochrome oxidase and acetylcholinesterase

Anderson, L.A.; Christianson, G.B.; Linden, J.F.

doi:10.1016/j.brainres.2008.11.037

Cited by 71Neuroscience and Music PerceptionNeuroscience and Neuropharmacology ResearchHearing, Cochlea, Tinnitus, Genetics

Mouse auditory cortex differs from visual and somatosensory cortices in the laminar distribution of cytochrome oxidase and acetylcholinesterase

Anderson, L.A., Christianson, G.B., Linden, J.F.·2009·Brain Research

DOI 10.1016/j.brainres.2008.11.037

Open this paper in CoChat — free account

Abstract

Cytochrome oxidase (CYO) and acetylcholinesterase (AChE) staining density varies across the cortical layers in many sensory areas. The laminar variations likely reflect differences between the layers in levels of metabolic activity and cholinergic modulation. The question of whether these laminar variations differ between primary sensory cortices has never been systematically addressed in the same set of animals, since most studies of sensory cortex focus on a single sensory modality. Here, we compared the laminar distribution of CYO and AChE activity in the primary auditory, visual, and somatosensory cortices of the mouse, using Nissl-stained sections to define laminar boundaries. Interestingly, for both CYO and AChE, laminar patterns of enzyme activity were similar in the visual and somatosensory cortices, but differed in the auditory cortex. In the visual and somatosensory areas, staining densities for both enzymes were highest in layers III/IV or IV and in lower layer V. In the auditory cortex, CYO activity showed a reliable peak only at the layer III/IV border, while AChE distribution was relatively homogeneous across layers. These results suggest that laminar patterns of metabolic activity and cholinergic influence are similar in the mouse visual and somatosensory cortices, but differ in the auditory cortex.

Integrity signals

Registry

Crossref · 10.1016/j.brainres.2008.11.037

Cites

76 of 76 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Auditory cortex was identified using hippocampal landmarks, a method previously validated using tonotopic mapping and dye injection.
“Auditory cortex was identified using hippocampal landmarks.This method has been previously validated using tonotopic mapping and dye injection (Martin del Campo et al. 2012) and comparison with the Paxinos mouse atlas and other publications on mouse auditory cortex (Anderson et al. 2009).”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Anderson et al. 2009

The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · see citing works
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258 · see citing works
The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex
Woolsey, T. A., & Van der Loos, H. (1970) · Brain Research · doi:10.1016/0006-8993(70)90079-x · Cited by 2,254 · see citing works
NEURONAL CIRCUITS OF THE NEOCORTEX
Douglas, R. J., & Martin, K. A. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144152 · Cited by 1,886 · see citing works
Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry
Wong‐Riley, M. T. T. (1979) · Brain Research · doi:10.1016/0006-8993(79)90728-5 · Cited by 1,853 · see citing works
Anatomy and physiology of a color system in the primate visual cortex
Livingstone, M. S., & Hubel, D. H. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00309.1984 · Cited by 1,637 · see citing works
Neuronal subtype specification in the cerebral cortex
Molyneaux, B. J., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2151 · Cited by 1,632 · see citing works
Cholinergic systems in mammalian brain and spinal cord
WOOLF, N. (1991) · Progress in Neurobiology · doi:10.1016/0301-0082(91)90006-m · Cited by 948 · see citing works
Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses
Zheng, Q. Y., Johnson, K. R., & Erway, L. C. (1999) · Hearing Research · doi:10.1016/s0378-5955(99)00003-9 · Cited by 832 · see citing works
Organization and morphological characteristics of cholonergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase
Houser, C. R., Crawford, G. D., Barber, R. P., Salvaterra, P. M., & Vaughn, J. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91312-4 · Cited by 748 · see citing works
Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans
Hackett, T. A., Preuss, T. M., & Kaas, J. H. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1407 · Cited by 522 · see citing works
Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys
Morel, A., Garraghty, P. E., & Kaas, J. H. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903350312 · Cited by 520 · see citing works
Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey
Horton, J. C., & Hubel, D. H. (1981) · Nature · doi:10.1038/292762a0 · Cited by 503 · see citing works
Perceptual Neuroscience: The Cerebral Cortex
Mountcastle, V. B. (1998) · Cited by 481 · see citing works
Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice.
Wong‐Riley, M. T. T., & Welt, C. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.4.2333 · Cited by 463 · see citing works
Architectonic map of neocortex of the normal mouse
Caviness, V. S. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901640207 · Cited by 448 · see citing works
The cerebral cortex of the rat
(1991) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(91)90172-9 · Cited by 416 · see citing works
Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex.
Livingstone, M. S., & Hubel, D. H. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.19.6098 · Cited by 343 · see citing works
Identification of central cholinergic neurons containing both choline acetyltransferase and acetylcholinesterase and of central neurons containing only acetylcholinesterase
Eckenstein, F. P., & Sofroniew, M. V. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-11-02286.1983 · Cited by 331 · see citing works
A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys
OʼKusky, J. R., & Colonnier, M. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902100307 · Cited by 327 · see citing works
The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation
Stiebler, I., Neulist, R., Fichtel, I., & Ehret, G. (1997) · Journal of Comparative Physiology A · doi:10.1007/s003590050140 · Cited by 316 · see citing works
A quantitative approach to cytoarchitectonics
Wree, A., Zilles, K., & Schleicher, A. (1981) · Anatomy and Embryology · doi:10.1007/bf00318096 · Cited by 300 · see citing works
Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons
Levey, A. I., Wainer, B. H., Rye, D. B., Mufson, E. J., & Mesulam, M. M. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90234-3 · Cited by 276 · see citing works
Cell structure and function in the visual cortex of the cat
Kelly, J. P., & Essen, D. C. V. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010541 · Cited by 265 · see citing works
Mapping Retinotopic Structure in Mouse Visual Cortex with Optical Imaging
Schuett, S., Bonhoeffer, T., & Hübener, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06549.2002 · Cited by 252 · see citing works
Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex
Horton, J. C., & Hedley‐Whyte, E. T. (1984) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1984.0022 · Cited by 241 · see citing works
An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex
Lysakowski, A., Wainer, B. H., Bruce, G., & Hersh, L. B. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90180-2 · Cited by 239 · see citing works
A Map of Visual Space Induced in Primary Auditory Cortex
Roe, A. W., Pallas, S. L., Hahm, J., & Sur, M. (1990) · Science · doi:10.1126/science.2237432 · Cited by 237 · see citing works
Cytochrome oxidase staining in the rat smI barrel cortex
Land, P., & Simons, D. (1985) · The Journal of comparative neurology · doi:10.1002/cne.902380209 · Cited by 224 · see citing works
Internet-enabled high-resolution brain mapping and virtual microscopy
Mikula, S., Trotts, I. J., Stone, J. M., & Jones, E. G. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.11.053 · Cited by 218 · see citing works
Acetylcholinesterase may have novel functions in the brain
Greenfield, S. A. (1984) · Trends in Neurosciences · doi:10.1016/s0166-2236(84)80055-7 · Cited by 216 · see citing works
Receptive field structure varies with layer in the primary visual cortex
Martinez, L. M., Wang, Q., Reid, R. C., Pillai, C., Alonso, J.-M., Sommer, F. T., & Hirsch, J. A. (2005) · Nature Neuroscience · doi:10.1038/nn1404 · Cited by 203 · see citing works
Stimulus-Dependent Neuronal Oscillations and Local Synchronization in Striate Cortex of the Alert Cat
Gray, C. M., & Prisco, G. V. D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-09-03239.1997 · Cited by 196 · see citing works
Histochemical identification of cortical areas in the auditory region of the human brain
Wallace, M. N., Johnston, P. W., & Palmer, A. R. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1014-z · Cited by 179 · see citing works
Cajal on the Cerebral Cortex: An Annotated Translation of the Complete Writings
Glickstein, M. (1989) · Annals of Internal Medicine · doi:10.7326/0003-4819-110-10-851_3 · Cited by 166 · see citing works
Functional organization in mouse barrel cortex
Simons, D. J., & Woolsey, T. A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90564-x · Cited by 165 · see citing works
Cytochrome oxidase activity in the auditory system of the mouse: A qualitative and quantitative histochemical study
Gonzalez-Lima, F., & Cada, A. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90550-9 · Cited by 163 · see citing works
Functional architecture of auditory cortex
Read, H. L. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00342-2 · Cited by 161 · see citing works
Columnar Transformations in Auditory Cortex? A Comparison to Visual and Somatosensory Cortices
Linden, J. F. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.1.83 · Cited by 149 · see citing works
Self-citation
A metabolic map of cytochrome oxidase in the rat brain: Histochemical, densitometric and biochemical studies
Hevner, R. F., Liu, S., & Wong‐Riley, M. T. T. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00514-6 · Cited by 147 · see citing works
Quantitative mapping of cytovhrome oxidase activity in the central auditory system of the gerbil: a study with calibrated activity standards and metal-intensified histochemistry
Gonzalez-Lima, F., & Jones, D. (1994) · Brain Research · doi:10.1016/0006-8993(94)90836-2 · Cited by 145 · see citing works
Somatosensory, auditory and visual cortical areas of the mouse.
Woolsey, T. A. (1967) · PubMed · Cited by 140 · see citing works
Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices
Smith, P. H., & Populin, L. C. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1084 · Cited by 128 · see citing works
Laminar distribution of receptive field properties in the primary visual cortex of the mouse
Mangini, N. J., & Pearlman, A. L. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901930114 · Cited by 127 · see citing works
Layer V in cat primary auditory cortex (AI): Cellular architecture and identification of projection neurons
Winer, J. A., & Prieto, J. J. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1183 · Cited by 121 · see citing works
Spectral integration in primary auditory cortex: Laminar processing of afferent input, in vivo and in vitro
Kaur, S., Rose, H. J., Lazar, R., Liang, K., & Metherate, R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.052 · Cited by 117 · see citing works
Development of cholinergic markers in mouse forebrain. I. Choline acetyltransferase enzyme activity and acetylcholinesterase histochemistry
Höhmann, C. F., & Ebner, F. F. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90045-8 · Cited by 112 · see citing works
Regional variations in cortical cholinergic innervation: Chemoarchitectonics of acetylcholinesterase-containing fibers in the macaque brain
Mesulam, M. M., Rosen, A. D., & Mufson, E. J. (1984) · Brain Research · doi:10.1016/0006-8993(84)90087-8 · Cited by 110 · see citing works
Cholinergic innervation of mouse forebrain structures
Kitt, C. A., Höhmann, C. F., COYLE, J. T., & Price, D. L. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410110 · Cited by 104 · see citing works
Acetylcholinesterase Staining in Human Auditory and Language Cortices: Regional Variation of Structural Features
Hutsler, J. J., & Gazzaniga, M. S. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.260 · Cited by 103 · see citing works
Overlap between acetylcholinesterase-rich and choline acetyltransferase-positive (cholinergic) axons in human cerebral cortex
Mesulam, M. M., & Geula, C. (1992) · Brain Research · doi:10.1016/0006-8993(92)90543-i · Cited by 93 · see citing works
Lis1–Nde1-dependent neuronal fate control determines cerebral cortical size and lamination
Pawlisz, A. S., Mutch, C. A., Wynshaw-Boris, A. J., Chenn, A., Walsh, C. A., & Feng, Y. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn144 · Cited by 89 · see citing works
Laminar differences in the response properties of cells in the primary auditory cortex
Wallace, M. N., & Palmer, A. R. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-1092-z · Cited by 87 · see citing works
Layer-Specific Touch-Dependent Facilitation and Depression in the Somatosensory Cortex during Active Whisking
Derdikman, D., Yu, C., Haidarliu, S., Bagdasarian, K., Arieli, A., & Ahissar, E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0918-06.2006 · Cited by 84 · see citing works
Primary auditory cortex in the rat: transient expression of acetylcholinesterase activity in developing geniculocortical projections
Robertson, R. T., Mostamand, F., Kageyama, G. H., Gallardo, K. A., & Yu, J. Z. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90240-j · Cited by 80 · see citing works
The pyramidal neurons in layer III of cat primary auditory cortex (AI)
Winer, J. A. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290404 · Cited by 77 · see citing works
<i>Zic</i>Deficiency in the Cortical Marginal Zone and Meninges Results in Cortical Lamination Defects Resembling Those in Type II Lissencephaly
Inoue, T., Ogawa, M., Mikoshiba, K., & Aruga, J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5735-07.2008 · Cited by 76 · see citing works
Sensory-evoked high-frequency (γ-band) oscillating potentials in somatosensory cortex of the unanesthetized rat
Jones, M. S., & Barth, D. S. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00639-2 · Cited by 74 · see citing works
Identification of subdivisions in the medial geniculate body of the guinea pig
Anderson, L. A., Wallace, M. N., & Palmer, A. R. (2007) · Hearing Research · doi:10.1016/j.heares.2007.02.005 · Cited by 66 · see citing works
Self-citation
Evoked Oscillations in the Thalamo-Cortical Auditory System Are Present in Anesthetized but not in Unanesthetized Rats
Cotillon, N., & Edeline, J. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00728.2002 · Cited by 66 · see citing works
The emergence of architectonic field structure and areal borders in developing monkey sensorimotor cortex
Huntley, G. W., & Jones, E. G. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90055-s · Cited by 65 · see citing works
Chemoarchitectonic organization of the cat primary auditory cortex
Wallace, M. N., Kitzes, L. M., & Jones, E. G. (1991) · Experimental Brain Research · doi:10.1007/bf00230525 · Cited by 54 · see citing works
The non‐pyramidal cells in layer III of cat primary auditory cortex (AI)
Winer, J. A. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290406 · Cited by 52 · see citing works
Laminar and cellular localization of cytochrome oxidase in the cat striate cortex
Kageyama, G. H., & Wong‐Riley, M. T. T. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902450202 · Cited by 51 · see citing works
Acetylcholinesterase and Neural Development: New Tricks for an Old Dog?
Robertson, R., & Yu, J. (1993) · Physiology · doi:10.1152/physiologyonline.1993.8.6.266 · Cited by 45 · see citing works
Lesions of the basal forebrain alter stimulus‐evoked metabolic activity in mouse somatosensory cortex
Ma, W., Höhmann, C. F., Coyle, J. T., & Juliano, S. L. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902880305 · Cited by 43 · see citing works
Acetylcholine innervation of sensory and motor neocortical areas in adult cat: a choline acetyltransferase immunohistochemical study
Avendaño, C., Umbriaco, D., Dykes, R. W., & Descarries, L. (1996) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(96)00132-9 · Cited by 42 · see citing works
A quantitative approach to cytoarchitectonics
Wree, A., Zilles, K., & Schleicher, A. (1983) · Anatomy and Embryology · doi:10.1007/bf00305922 · Cited by 40 · see citing works
Area 3a in the cat. I. A reevaluation of its location and architecture on the basis of Nissl, myelin, acetylcholinesterase, and cytochrome oxidase staining
Avendaño, C., & Verdú, A. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210305 · Cited by 31 · see citing works
Hierarchy within human SI: supporting data from cytochrome oxidase, acetylcholinesterase and NADPH-diaphorase staining patterns
Eskenasy, S. C. A.-C. C. (2000) · Somatosensory & Motor Research · doi:10.1080/08990220050020544 · Cited by 17 · see citing works
Designer channels: site-directed mutagenesis as a probe for structural features of channels and receptors
White, M. M. (1985) · Trends in Neurosciences · doi:10.1016/0166-2236(85)90124-9 · Cited by 15 · see citing works
Regional variations of cytochrome oxidase activity in the central auditory system of Relnrl-Orl (reeler) mutant mice
Hayzoun, K., Lalonde, R., Mariani, J., & Strazielle, C. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.04.008 · Cited by 5 · see citing works

Flagged first, then by citations

Sorted by citations

Parvalbumin-Expressing Inhibitory Interneurons in Auditory Cortex Are Well-Tuned for Frequency
Moore, A. K., & Wehr, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0663-13.2013 · Cited by 225 · see citing works
Stimulus-Specific Adaptation Occurs in the Auditory Thalamus
Anderson, L. A., Christianson, G. B., & Linden, J. F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0793-09.2009 · Cited by 232 · see citing works
Self-citation
Robustness of Cortical Topography across Fields, Laminae, Anesthetic States, and Neurophysiological Signal Types
Guo, W., Chambers, A. R., Darrow, K. N., Hancock, K. E., Shinn‐Cunningham, B. G., & Polley, D. B. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0065-12.2012 · Cited by 226 · see citing works
In vivo Stimulus-Induced Vasodilation Occurs without IP 3 Receptor Activation and May Precede Astrocytic Calcium Increase
Nizar, K., Uhlířová, H., Tian, P., Saisan, P. A., Cheng, Q., Reznichenko, L., Weldy, K. L., Steed, T., Sridhar, V. B., MacDonald, C. L., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3285-12.2013 · Cited by 220 · see citing works
Mechanical failure modes of chronically implanted planar silicon-based neural probes for laminar recording
Kozai, T. D. Y., Catt, K. A., Li, X., Gugel, Z. V., Olafsson, V. T., Vazquez, A. L., & Cui, X. T. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.040 · Cited by 214 · see citing works
Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice
Wen, T. H., Afroz, S., Reinhard, S. M., Palacios, A. R., Tapia, K., Binder, D. K., Razak, K. A., & Ethell, I. M. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhx258 · Cited by 165 · see citing works
Altered auditory processing in a mouse model of fragile X syndrome
Rotschafer, S. E., & Razak, K. A. (2013) · Brain Research · doi:10.1016/j.brainres.2013.02.038 · Cited by 138 · see citing works
Attenuation of responses to self-generated sounds in auditory cortical neurons
Rummell, B. P., Klee, J. L., & Sigurdsson, T. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1564-16.2016 · Cited by 103 · see citing works
Physiological differences between histologically defined subdivisions in the mouse auditory thalamus
Anderson, L. A., & Linden, J. F. (2010) · Hearing Research · doi:10.1016/j.heares.2010.12.016 · Cited by 103 · see citing works
Self-citation
The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits
Oviedo, H. V., Bureau, I., Svoboda, K., & Zador, A. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2659 · Cited by 100 · see citing works
Rapid Rebalancing of Excitation and Inhibition by Cortical Circuitry
Moore, A. K., Weible, A. P., Balmer, T. S., Trussell, L. O., & Wehr, M. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.045 · Cited by 93 · see citing works
Deletion of Fmr1 from Forebrain Excitatory Neurons Triggers Abnormal Cellular, EEG, and Behavioral Phenotypes in the Auditory Cortex of a Mouse Model of Fragile X Syndrome
Lovelace, J. W., Rais, M., Palacios, A. R., Shuai, X. S., Bishay, S., Popa, O., Pirbhoy, P. S., Binder, D. K., Nelson, D. L., Ethell, I. M., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz141 · Cited by 81 · see citing works
Parvalbumin immunoreactivity in the auditory cortex of a mouse model of presbycusis.
Martin del Campo, H. N., Measor, K. R., & Razak, K. A. (2012) · Hearing Research · doi:10.1016/j.heares.2012.08.017 · Cited by 76 · see citing works
Primary Auditory Cortex is Required for Anticipatory Motor Response
Li, J., Liao, X., Zhang, J., Wang, M., Yang, N., Zhang, J., Lv, G., Li, H., Lu, J., Ding, R., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx079 · Cited by 73 · see citing works
In Vivo Functional Mapping of a Cortical Column at Single-Neuron Resolution
Tischbirek, C. H., Noda, T., Tohmi, M., Birkner, A., Nelken, I., & Konnerth, A. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.007 · Cited by 66 · see citing works
Two populations of corticothalamic and interareal corticocortical cells in the subgranular layers of the mouse primary sensory cortices
Petrof, I., Viaene, A. N., & Sherman, S. M. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.23006 · Cited by 62 · see citing works
Acute pharmacological inhibition of matrix metalloproteinase‐9 activity during development restores perineuronal net formation and normalizes auditory processing in <i>Fmr1</i> KO mice
Pirbhoy, P. S., Rais, M., Lovelace, J. W., Woodard, W., Razak, K. A., Binder, D. K., & Ethell, I. M. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15037 · Cited by 62 · see citing works
The insular auditory field receives input from the lemniscal subdivision of the auditory thalamus in mice
Takemoto, M., Hasegawa, K., Nishimura, M., & Song, W. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23491 · Cited by 61 · see citing works
Circuit asymmetries underlie functional lateralization in the mouse auditory cortex
Levy, R. B., Marquarding, T., Reid, A. P., Pun, C. M., Renier, N., & Oviedo, H. V. (2019) · Nature Communications · doi:10.1038/s41467-019-10690-3 · Cited by 59 · see citing works
Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice
Brewton, D. H., Kokash, J., Jimenez, O., Pena, E. R., & Razak, K. A. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00270 · Cited by 54 · see citing works
Local and Global Spatial Organization of Interaural Level Difference and Frequency Preferences in Auditory Cortex
Panniello, M., King, A. J., Dahmen, J. C., & Walker, K. M. M. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx295 · Cited by 48 · see citing works
Neocortex
Kirkcaldie, M. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10004-4 · Cited by 40 · see citing works
Effects of noise-induced hearing loss on parvalbumin and perineuronal net expression in the mouse primary auditory cortex
Nguyen, A., Khaleel, H. M., & Razak, K. A. (2017) · Hearing Research · doi:10.1016/j.heares.2017.04.015 · Cited by 36 · see citing works
Depth-Dependent Temporal Response Properties in Core Auditory Cortex
Christianson, G. B., Sahani, M., & Linden, J. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2863-11.2011 · Cited by 36 · see citing works
Self-citation
Selectivity for the rate of frequency-modulated sweeps in the mouse auditory cortex
Trujillo, M. S., Measor, K., Carrasco, M. M., & Razak, K. A. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00480.2011 · Cited by 37 · see citing works
Modulatory compartments in cortex and local regulation of cholinergic tone
Coppola, J. J., Ward, N. J., Jadi, M. P., & Disney, A. A. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.08.001 · Cited by 35 · see citing works
Contrast gain control in mouse auditory cortex
Cooke, J. E., King, A. J., Willmore, B. D. B., & Schnupp, J. W. H. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00847.2017 · Cited by 32 · see citing works
Differential maturation of vesicular glutamate and GABA transporter expression in the mouse auditory forebrain during the first weeks of hearing
Hackett, T. A., Clause, A. R., Takahata, T., Hackett, N., & Polley, D. B. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1062-3 · Cited by 34 · see citing works
Reduced perineuronal net expression in Fmr1 KO mice auditory cortex and amygdala is linked to impaired fear-associated memory
Reinhard, S. M., Rais, M., Afroz, S., Hanania, Y., Pendi, K., Espinoza, K., Rosenthal, R., Binder, D. K., Ethell, I. M., & Razak, K. A. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107042 · Cited by 33 · see citing works
Complexity of frequency receptive fields predicts tonotopic variability across species
Gaucher, Q., Panniello, M., Ivanov, A. Z., Dahmen, J. C., King, A. J., & Walker, K. M. M. (2020) · eLife · doi:10.7554/elife.53462 · Cited by 28 · see citing works
Chrna5 is Essential for a Rapid and Protected Response to Optogenetic Release of Endogenous Acetylcholine in Prefrontal Cortex
Venkatesan, S., & Lambe, E. K. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1128-20.2020 · Cited by 30 · see citing works
Beneficial effects of sound exposure on auditory cortex development in a mouse model of Fragile X Syndrome.
Kulinich, A., Reinhard, S. M., Rais, M., Lovelace, J., Scott, V., Binder, D., Razak, K., & Ethell, I. M. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104622 · Cited by 27 · see citing works
Close temporal coupling of neuronal activity and tissue oxygen responses in rodent whisker barrel cortex
Li, J., Bravo, D. S., Upton, A. L., Gilmour, G., Tricklebank, M. D., Fillenz, M., Martin, C. J., Lowry, J. P., Bannerman, D. M., & McHugh, S. B. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07927.x · Cited by 29 · see citing works
Nicotinic neuromodulation in auditory cortex requires MAPK activation in thalamocortical and intracortical circuits
Intskirveli, I., & Metherate, R. (2012) · Journal of Neurophysiology · doi:10.1152/jn.01129.2011 · Cited by 29 · see citing works
Heightened Nicotinic Regulation of Auditory Cortex during Adolescence
Kawai, H. D., Kang, H.-A., & Metherate, R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1705-11.2011 · Cited by 25 · see citing works
A characterization of laminar architecture in mouse primary auditory cortex
Chang, M., & Kawai, H. D. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1744-8 · Cited by 25 · see citing works
Effects of Locomotion in Auditory Cortex Are Not Mediated by the VIP Network
Yavorska, I., & Wehr, M. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.618881 · Cited by 24 · see citing works
Functional consequences of postnatal interventions in a mouse model of Fragile X syndrome
Rais, M., Lovelace, J. W., Shuai, X. S., Woodard, W., Bishay, S., Estrada, L., Sharma, A. R., Nguy, A. K., Kulinich, A. O., Pirbhoy, P. S., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105577 · Cited by 22 · see citing works
The cholinergic basal forebrain in the ferret and its inputs to the auditory cortex
Bajo, V. M., Leach, N. D., Cordery, P. M., Nodal, F. R., & King, A. J. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12653 · Cited by 21 · see citing works
Endogenous Acetylcholine and Its Modulation of Cortical Microcircuits to Enhance Cognition
Venkatesan, S., Jeoung, H., Chen, T., Power, S. K., Liu, Y., & Lambe, E. K. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_138 · Cited by 21 · see citing works
Knowledge About Sounds—Context-Specific Meaning Differently Activates Cortical Hemispheres, Auditory Cortical Fields, and Layers in House Mice
Geissler, D. B., Schmidt, H. S., & Ehret, G. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00098 · Cited by 19 · see citing works
Laminar specific gene expression reveals differences in postnatal laminar maturation in mouse auditory, visual, and somatosensory cortex
Chang, M., Suzuki, N., & Kawai, H. D. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24481 · Cited by 17 · see citing works
Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex
Liu, T., Petrof, I., & Sherman, S. M. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00730.2013 · Cited by 17 · see citing works
Adenosine A1 Receptor mRNA Expression by Neurons and Glia in the Auditory Forebrain
Hackett, T. A. (2018) · The Anatomical Record · doi:10.1002/ar.23907 · Cited by 16 · see citing works
Effects of developmental noise exposure on inhibitory cell densities and perineuronal nets in A1 and AAF of mice
Reinhard, S. M., Abundez-Toledo, M., Espinoza, K., & Razak, K. A. (2019) · Hearing Research · doi:10.1016/j.heares.2019.107781 · Cited by 15 · see citing works
Arc/Arg3.1 mRNA expression reveals a subcellular trace of prior sound exposure in adult primary auditory cortex
Ivanova, T. N., Matthews, A., Gross, C., Mappus, R. C., Gollnick, C., Swanson, A., Bassell, G. J., & Liu, R. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.02.034 · Cited by 14 · see citing works
Enhanced Discriminative Abilities of Auditory Cortex Neurons for Pup Calls Despite Reduced Evoked Responses in C57BL/6 Mother Mice
Royer, J., Huetz, C., Occelli, F., Cancela, J., & Edeline, J. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.11.031 · Cited by 12 · see citing works
Amyloid Pathology in the Central Auditory Pathway of 5XFAD Mice Appears First in Auditory Cortex
Weible, A. P., & Wehr, M. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220538 · Cited by 11 · see citing works
Muscarinic acetylcholine receptor-dependent persistent activity of layer 5 intrinsic-bursting and regular-spiking neurons in primary auditory cortex
Fu, X., Ye, H., Jia, H., Wang, X., Chomiak, T., & Luo, F. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00184.2019 · Cited by 10 · see citing works
A Layer 3→5 Circuit in Auditory Cortex That Contributes to Pre-pulse Inhibition of the Acoustic Startle Response
Weible, A. P., Yavorska, I., Kayal, D., Duckler, U., & Wehr, M. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.553208 · Cited by 9 · see citing works
Resveratrol prevents hearing loss and a subregion specific- reduction of serotonin reuptake transporter induced by noise exposure in the central auditory system
Cheng, L.-Q., Shu, F.-Q., Zhang, M., Kai, Y.-Z., & Tang, Z. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1134153 · Cited by 7 · see citing works
Laminar Organization of FM Direction Selectivity in the Primary Auditory Cortex of the Free-Tailed Bat
Macías, S., Bakshi, K., & Smotherman, M. S. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00076 · Cited by 7 · see citing works
Effects of M currents on the persistent activity of pyramidal neurons in mouse primary auditory cortex
Ye, H., Liu, Z.-X., He, Y.-J., & Wang, X. (2022) · Journal of Neurophysiology · doi:10.1152/jn.00332.2021 · Cited by 6 · see citing works
Convergence of nicotine-induced and auditory-evoked neural activity activates ERK in auditory cortex
Kawai, H. D., La, M., Kang, H.-A., Hashimoto, Y., Liang, K., Lazar, R., & Metherate, R. (2013) · Synapse · doi:10.1002/syn.21647 · Cited by 5 · see citing works
Alpha-2 nicotinic acetylcholine receptors regulate spectral integration in auditory cortex
Intskirveli, I., Gil, S. M., Lazar, R., & Metherate, R. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1492452 · Cited by 3 · see citing works
Familiarity with a vocal category biases the compartmental expression ofArc/Arg3.1in core auditory cortexPreprint
Ivanova, T. N., Groß, C., Mappus, R. C., Kwon, Y. J., Bassell, G. J., & Liu, R. C. (2017) · Learning & Memory · doi:10.1101/lm.046086.117 · Cited by 3 · see citing works
Differential effects of sound repetition rate on auditory cortex development and behavior in fragile X syndrome mouse model
Norman, A. O., Farooq, N., Sahni, A., Tapia, K., Breiner, D., Razak, K. A., & Ethell, I. M. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115184 · Cited by 2 · see citing works
Ketamine does not rescue plaque load or gap detection in the 5XFAD mouse model of Alzheimer's disease
Wright, A. L., Weible, A. P., Estes, O. B., & Wehr, M. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1505908 · Cited by 2 · see citing works
Spectral and Temporal Acoustic Features Modulate Response Irregularities within Primary Auditory Cortex Columns
Carrasco, A. E., Brown, T. A., & Lomber, S. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114550 · Cited by 2 · see citing works
Columnar and layer-specific representation of spatial sensitivity in mouse primary auditory cortex
Yuan, K., & Shen, J. (2011) · Neuroreport · doi:10.1097/wnr.0b013e328348aae5 · Cited by 2 · see citing works
Untitled work
Rais (2022) · doi:10.1101/2022.02.08.479618 · Cited by 2 · see citing works
Physiological differences between histologically identified subdivisions in the mouse auditory thalamus
Anderson, L. A., & Linden, J. F. (2011) · UCL Discovery (University College London)
Self-citation
Layer-specific modulation of neuronal excitability by 660-nm laser irradiation in mouse neocortex
Kumazaki, K., Mieda, T., Kogure, S., & Kawai, H. D. (2013) · Lasers in Medical Science · doi:10.1007/s10103-013-1484-1
Gap Detection in Auditory Cortex
Duckler, U. (2016) · Scholars' Bank (University of Oregon)
Circuits for active vision : parallel tectothalamocortical visual pathways in the mouse.
Zhou, N. (2017) · doi:10.18297/etd/2782
A genetically identified population of layer 4 neurons in auditory cortex that contributes to pre-pulse inhibition of the acoustic startle response
Weible, A. P., Yavorska, I., Narayanan, A., & Wehr, M. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.972157
Cytoarchitecture and myeloarchitecture of the sheep auditory cortex
Pluchot, C., Morisse, M., Meurisse, M., Graïc, J., Chaillou, É., & Love, S. (2025) · Journal of Anatomy · doi:10.1111/joa.70072
The influence of statistical context on the neural representation of sound
Williamson, R. S. (2012) · UCL Discovery (University College London)
Étude électrophysiologique et bi-photonique des modifications du traitement des signaux de communication dans le cortex auditif chez des souris mères n’exprimant pas de canaux endolysosomaux « two-pore channels » (TPC)
Royer, J. (2021) · theses.fr (ABES) · doi:10.70675/9561320dz3197z4755zbb24zf51613d38d02
Hyperpolarized 13C-bicarbonate production correlates with excitatory neuron distribution in the human brain
Uthayakumar, B., Dingwell, D. A., Cappelletto, N. I. C., Bragagnolo, N. D., Chen, A. P., Ma, N., Endre, R., Gillis, J. A., Soliman, H., & Cunningham, C. H. (2026) · Imaging Neuroscience · doi:10.1162/imag.a.1342
Chronic nicotine reverses age-related decline of interneuron markers in mouse auditory cortex
Intskirveli, I., Lazar, R., Hidalgo, D., & Metherate, R. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1876409

Compartments within human primary auditory cortex: evidence from cytochrome oxidase and acetylcholinesterase staining
Clarke, S., & Rivier, F. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00043.x · Cited by 59 · see citing works
Acetylcholinesterase Staining in Human Auditory and Language Cortices: Regional Variation of Structural Features
Hutsler, J. J., & Gazzaniga, M. S. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.2.260 · Cited by 103 · see citing works
Cytochrome oxidase activity in the auditory system of the mouse: A qualitative and quantitative histochemical study
Gonzalez-Lima, F., & Cada, A. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90550-9 · Cited by 163 · see citing works
Distribution of acetylcholinesterase and zinc in the visual cortex of the mouse
Garrett, B., Geneser, F. A., & Slomianka, L. (1991) · Anatomy and Embryology · doi:10.1007/bf01236052 · Cited by 21 · see citing works
Laminar Distribution of Cytochrome Oxidase Staining in Cetacean Isocortex
Revishchin, A. V., & Garey, L. J. (2008) · Brain Behavior and Evolution · doi:10.1159/000114370 · Cited by 14 · see citing works

Authors: Anderson, L. A., Christianson, G. B., & Linden, J. F.
Affiliations: University College London (GB)
Corresponding author: Linden, J.F.
ORCID: Anderson, L.A.
Linden, J.F.
Venue: Brain Research
Publisher: Elsevier BV
Published: 2009-02
Volume: 1252
Pages: 130-142
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/j.brainres.2008.11.037
OpenAlex: W2026998078
Cited by: 71
References: 76
Citations by year: 2026: 2 · 2025: 3 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 3 · 2020: 6 · 2019: 8 · 2018: 5 · 2017: 6 · 2016: 5 · 2015: 1 · 2014: 4 · 2013: 6 · 2012: 4
FWCI: 2.07
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Brain Research (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
Keywords: auditory cortex, visual cortex, somatosensory cortex, cytochrome c oxidase, acetylcholinesterase, cortical laminar distribution, cholinergic modulation, primary sensory cortices, mouse brain
MeSH terms: Acetylcholinesterase, Age Factors, Animals, Auditory Cortex, Cerebral Cortex, Electron Transport Complex IV, Densitometry, Female, Male, Mice, Inbred CBA, Mothers, Somatosensory Cortex, Visual Cortex, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Mouse auditory cortex differs from visual and somatosensory cortices in the laminar distribution of cytochrome oxidase and acetylcholinesterase

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks