Evidence for nonreciprocal organization of the mouse auditory thalamocortical‐corticothalamic projection systems

Llano, Daniel A.; Sherman, S. Murray

doi:10.1002/cne.21602

Cited by 186Neuroscience and Music PerceptionHearing, Cochlea, Tinnitus, GeneticsNeuroscience and Neuropharmacology Research

Evidence for nonreciprocal organization of the mouse auditory thalamocortical‐corticothalamic projection systems

Llano, Daniel A., Sherman, S. Murray·2008·Journal of Comparative Neurology

DOI 10.1002/cne.21602

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Abstract

We tested the hypothesis that information is routed from one area of the auditory cortex (AC) to another via the dorsal division of the medial geniculate body (MGBd) by analyzing the degree of reciprocal connectivity between the auditory thalamus and cortex. Biotinylated dextran amine injected into the primary AC (AI) or anterior auditory field (AAF) of mice produced large, “driver‐type” terminals primarily in the MGBd, with essentially no such terminals in the ventral MGB (MGBv). In contrast, small, “modulator‐type” terminals were found primarily in the MGBv, and this coincided with areas of retrogradely labeled thalamocortical cell bodies. After MGBv injections, anterograde label was observed in layers 4 and 6 of the AI and AAF, which coincided with retrogradely labeled layer 6 cell bodies. After MGBd injections, thalamocortical terminals were seen in layers 1, 4, and 6 of the secondary AC and dorsoposterior AC, which coincided with labeled layer 6 cell bodies. Notably, after MGBd injection, a substantial number of layer 5 cells were labeled in all AC areas, whereas very few were seen after MGBv injection. Further, the degree of anterograde label in layer 4 of cortical columns containing labeled layer 6 cell bodies was greater than in columns containing labeled layer 5 cell bodies. These data suggest that auditory layer 5 corticothalamic projections are targeted to the MGBd in a nonreciprocal fashion and that the MGBd may route this information to the nonprimary AC. J. Comp. Neurol. 507:1209–1227, 2008. © 2008 Wiley‐Liss, Inc.

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Further evidence for two types of corticopulvinar neurons
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Bidirectional movement of horseradish peroxidase and the demonstration of reciprocal thalamocortical connections
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A distinct ultrasound-processing area in the auditory cortex of the mouse
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Nuclear respiratory factor-2 subunit protein: Correlation with cytochrome oxydase and regulation by functional activity in the monkey primary visual cortex
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Microtopography of the dual corticothalamic projections originating from domains along the frequency axis of the cat primary auditory cortex
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Response characteristics of neurons in the medial geniculate body of the little brown bat to simple and temporally-patterned sounds
Llano, D. A., & Feng, A. S. (1999) · Journal of Comparative Physiology A · doi:10.1007/s003590050336 · Cited by 15 · see citing works
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Functional organization of the auditory cortex in a native Chilean rodent (Octodon degus).
Thomas, H. C., & Tillein, J. (1997) · PubMed · Cited by 14 · see citing works
Abnormal retinotopic organization of the dorsal lateral geniculate nucleus of the tyrosinase-negative albino cat
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Divergence and collateral axon branching in subsystems of visual cortical projections from the cat lateral posterior nucleus.
Miceli, D., Repérant, J., Marchand, L., Ward, R. M., & Vesselkin, N. P. (1991) · PubMed · Cited by 13 · see citing works
Untitled work
Hagihara (1999) · doi:10.1002/(sici)1096-9861(19990726)410:2

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A mesoscale connectome of the mouse brain
Oh, S. W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M., et al. (2014) · Nature · doi:10.1038/nature13186 · Cited by 2,612 · see citing works
Functional organization and population dynamics in the mouse primary auditory cortex
Rothschild, G., Nelken, I., & Mizrahi, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2484 · Cited by 390 · see citing works
The corticothalamocortical circuit drives higher-order cortex in the mouse
Theyel, B. B., Llano, D. A., & Sherman, S. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2449 · Cited by 366 · see citing works
Self-citation
Distinct functions for direct and transthalamic corticocortical connections
Sherman, S. M., & Guillery, R. W. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00429.2011 · Cited by 336 · see citing works
Self-citation
Neocortical layer 6, a review
Thomson (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00013 · Cited by 269 · see citing works
“Primary auditory cortico-thalamic connections exhibit similar differences between the projections from layers 5 and upper and lower layer 6 to those seen in the visual system (Ojima, 1994; Llano and Sherman, 2008).”
Thalamocortical Innervation Pattern in Mouse Auditory and Visual Cortex: Laminar and Cell-Type Specificity
Ji, X.-Y., Zingg, B., Mesik, L., Xiao, Z., Zhang, L. I., & Tao, H. W. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv099 · Cited by 176 · see citing works
A Corticothalamic Circuit for Dynamic Switching between Feature Detection and Discrimination
Guo, W., Clause, A. R., Barth‐Maron, A., & Polley, D. B. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.019 · Cited by 179 · see citing works
“…to the thalamus and dense local connectivity with excitatory and inhibitory neurons within the cortical column (Bortone et al., 2014; Bourassa and Deschênes, 1995; Briggs et al., 2016; Llano and Sherman, 2008; Winer et al., 2001; Zhang and Deschênes, 1997; S. Ramon y Cajal, 1906 Nobel lecture).”
Thalamic mechanisms in language: A reconsideration based on recent findings and concepts
Crosson, B. (2012) · Brain and Language · doi:10.1016/j.bandl.2012.06.011 · Cited by 167 · see citing works
“In mice, Llano and Sherman (2008) investigated connections between primary and closely associated auditory cortex (A1 and anterior auditory field (AAF), respectively), the dorsal and ventral divisions of the medial geniculate body (MGBd and MGBv, respectively), and secondary and closely associated auditory cortex (A2…”
Influential
The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: a potential neuronal correlate for predictive coding
Malmierca, M. S., Anderson, L. A., & Antunes, F. M. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00019 · Cited by 159 · see citing works
“Recent modeling studies (Lieder et al., 2013) suggested that the MMN reflects approximate Bayesian learning of sensory regularities, and that the MMN-generating process adjusts a probabilistic model of the environment according to mismatch responses (prediction errors).”
BackgroundMethodInfluential
Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse
Viaene, A. N., Petrof, I., & Sherman, S. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114828108 · Cited by 157 · see citing works
Self-citation
Functioning of Circuits Connecting Thalamus and Cortex
Sherman, S. M. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160032 · Cited by 163 · see citing works
Self-citation
Synaptic Properties of Thalamic Input to Layers 2/3 and 4 of Primary Somatosensory and Auditory Cortices
Viaene, A. N., Petrof, I., & Sherman, S. M. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00747.2010 · Cited by 138 · see citing works
“Given the limits of the resolution at the light microscopic level with our combination of magnification and numerical aperture have been estimated to be around 0.3 m (Friedlander et al. 1981; Llano and Sherman 2008; Slayter 1970).”
InfluentialSelf-citation
Synaptic properties of connections between the primary and secondary auditory cortices in mice
Covic, E. N., & Sherman, S. M. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr029 · Cited by 116 · see citing works
Self-citation
The organization and physiology of the auditory thalamus and its role in processing acoustic features important for speech perception
Bartlett, E. L. (2013) · Brain and Language · doi:10.1016/j.bandl.2013.03.003 · Cited by 118 · see citing works
“4A), such that regions in MGV that project to a given area of auditory cortex are likely to receive significant corticothalamic feedback from layer 6 neurons of that area of cortex (Winer et al. 2001, Kimura et al. 2005, Llano and Sherman 2008).”
Background
Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
Liu, J., Whiteway, M. R., Sheikhattar, A., Butts, D. A., Babadi, B., & Kanold, P. O. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.069 · Cited by 117 · see citing works
“This is also consistent with the laminar targets of lemniscal and non-lemniscal MGB afferents with the latter being present in L1 (Llano and Sherman, 2008; Saldeitis et al., 2014) and with that L5/6 neurons were less likely to generate Off-R (Volkov and Galazjuk, 1991).”
BackgroundResult
Parallel pathways for sound processing and functional connectivity among layer 5 and 6 auditory corticofugal neurons
Williamson, R. S., & Polley, D. B. (2019) · eLife · doi:10.7554/elife.42974 · Cited by 114 · see citing works
“307 Most L5 CF neurons fall into the class of L5 pyramidal neurons referred to as intrinsic bursting 308 (IB), based on their tendency to fire bursts of action potentials in response to depolarizing current 309 injection (Connors et al., 1982; McCormick et al., 1985; Llano and Sherman, 2008; Joshi et al., 310 2015).”
Background
Topography and physiology of ascending streams in the auditory tectothalamic pathway
Lee, C. C., & Sherman, S. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907873107 · Cited by 110 · see citing works
“, large terminals that synapse on proximal dendrites) (6).”
BackgroundSelf-citation
A Layer-specific Corticofugal Input to the Mouse Superior Colliculus
Zurita, H., Rock, C., Perkins, J., & Apicella, A. J. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx161 · Cited by 107 · see citing works
Differences in Intrinsic Properties and Local Network Connectivity of Identified Layer 5 and Layer 6 Adult Mouse Auditory Corticothalamic Neurons Support a Dual Corticothalamic Projection Hypothesis
Llano, D. A., & Sherman, S. M. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp050 · Cited by 96 · see citing works
“Layer 5 and Layer 6 Adult Mouse Auditory”
BackgroundInfluentialSelf-citation
Descending Connections of Auditory Cortex to the Midbrain and Brain Stem
Malmierca, M. S., & Ryugo, D. K. (2010) · Springer eBooks · doi:10.1007/978-1-4419-0074-6_9 · Cited by 95 · see citing works
Preceding Inhibition Silences Layer 6 Neurons in Auditory Cortex
Zhou, Y., Liu, B., Wu, G. K., Kim, Y.-J., Xiao, Z., Tao, H. W., & Zhang, L. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.021 · Cited by 94 · see citing works
“Conversely, L6 in various primary sensory cortices sends feedback projections predominantly to the first-order thalamic nucleus (i.e., ventral MGB of the auditory thalamus, MGBv) (Ojima, 1994; Prieto and Winer, 1999; Winer, 2005; Takayanagi and Ojima, 2006; Rouiller and Welker, 2000; Llano and Sherman, 2008), whereas…”
Influential
Diminished Cortical Inhibition in an Aging Mouse Model of Chronic Tinnitus
Llano, D. A., Turner, J. G., & Caspary, D. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2499-12.2012 · Cited by 93 · see citing works
“Previous work suggested that these markers separate primary auditory fields (primary auditory cortex and anterior auditory field) from nonprimary fields (Caviness, 1975; Wallace et al., 1991; Molinari et al., 1995; Budinger et al., 2000; Cruikshank et al., 2001; Llano and Sherman, 2008) Slices were stored in 4% parafo…”
BackgroundMethodSelf-citation
Connections of Auditory and Visual Cortex in the Prairie Vole (Microtus ochrogaster): Evidence for Multisensory Processing in Primary Sensory Areas
Campi, K. L., Bales, K. L., Grunewald, R., & Krubitzer, L. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp082 · Cited by 93 · see citing works
Auditory thalamic circuits and GABAA receptor function: Putative mechanisms in tinnitus pathology
Caspary, D. M., & Llano, D. A. (2016) · Hearing Research · doi:10.1016/j.heares.2016.08.009 · Cited by 90 · see citing works
“…divisions of the MGB show poor tonotopic order and are considered non-lemniscal (see Bartlett, 2013), receiving inputs from the non-tonotopically organized regions of the inferior colliculus (Calford & Aitkin, 1983) as well as driver-like input from the auditory cortex (Llano & Sherman, 2008).”
Self-citation
The auditory corticocollicular system: Molecular and circuit-level considerations
Stebbings, K. A., Lesicko, A. M. H., & Llano, D. A. (2014) · Hearing Research · doi:10.1016/j.heares.2014.05.004 · Cited by 84 · see citing works
“…in different cortical subnetworks, have different intrinsic properties, different patterns of projections to the thalamus, and possibly, different roles in shaping thalamic function (Ojima, 1994; Reichova and Sherman, 2004; Llano and Sherman, 2008; Llano and Sherman, 2009; Theyel et al., 2010).”
BackgroundSelf-citation
Layer 5 Corticofugal Projections from Diverse Cortical Areas: Variations on a Pattern of Thalamic and Extrathalamic Targets
Prasad, J. A., Carroll, B. J., & Sherman, S. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0529-20.2020 · Cited by 82 · see citing works
“While L5 projections are characterized as including both large and small terminal populations, L6 corticothalamic terminals are exclusively small (Van Horn and Sherman, 2004; Llano and Sherman, 2008; Sherman and Guillery, 2013).”
BackgroundSelf-citation
Auditory Corticothalamic Neurons Are Recruited by Motor Preparatory Inputs
Clayton, K. K., Williamson, R. S., Hancock, K. E., Tasaka, G., Mizrahi, A., Hackett, T. A., & Polley, D. B. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.027 · Cited by 82 · see citing works
On the classification of pathways in the auditory midbrain, thalamus, and cortex
Lee, C. C., & Sherman, S. M. (2010) · Hearing Research · doi:10.1016/j.heares.2010.12.012 · Cited by 80 · see citing works
“By comparison, Class 2 inputs, like the layer 6 corticothalamic projection, have thin axons, sparse arbors, and small terminals ending on distal dendrites (Bartlett and Smith, 1999; Llano and Sherman, 2008; Sherman and Guillery, 2006; Smith et al., 2007).”
BackgroundInfluentialSelf-citation
Medial geniculate body and primary auditory cortex differentially contribute to striatal sound representations
Chen, L., Wang, X., Ge, S., & Xiong, Q. (2019) · Nature Communications · doi:10.1038/s41467-019-08350-7 · Cited by 75 · see citing works
Corticothalamic pathways in auditory processing: recent advances and insights from other sensory systems
Antunes, F. M., & Malmierca, M. S. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.721186 · Cited by 71 · 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
Single-neuron representation of learned complex sounds in the auditory cortex
Wang, M., Liao, X., Li, R., Liang, S., Ding, R., Li, J., Zhang, J., He, W., Liu, K., Pan, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18142-z · Cited by 71 · see citing works
Exploring functions for the non-lemniscal auditory thalamus
Lee, C. C. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00069 · Cited by 63 · see citing works
“Such synapses then, despite their numerical minority, can exert a potent influence on their postsynaptic targets, much like the numerically sparse retinogeniculate projection (Sherman and Guillery, 1998; Winer et al., 1999; Bartlett et al., 2000; Llano and Sherman, 2008).”
BackgroundInfluential
Thalamic and cortical pathways supporting auditory processing
Lee, C. C. (2012) · Brain and Language · doi:10.1016/j.bandl.2012.05.004 · Cited by 70 · see citing works
“…from layer 5 of the primary auditory cortex to the dorsal division of the MGB (Bajo et al., 1995; Cappe, Morel, Barone, & Rouiller, 2009; Llano & Sherman, 2008; Ojima, 1994; Winer, Larue, & Huang, 1999) establish a potential alternate route for information flow between cortical areas,…”
BackgroundInfluential
Delineation of a frequency-organized region isolated from the mouse primary auditory cortex
Tsukano, H., Horie, M., Bo, T., Uchimura, A., Hishida, R., Kudoh, M., Takahashi, K., Takebayashi, H., & Shibuki, K. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00932.2014 · Cited by 69 · see citing works
Drivers and modulators in the central auditory pathways
Lee, C. C. (2010) · Frontiers in Neuroscience · doi:10.3389/neuro.01.014.2010 · Cited by 68 · see citing works
“Morphologically, these thalamocortical projections have large, dense, bushy arborizations in layer 4 that extend into layer 3 (Huang and Winer, 2000; Llano and Sherman, 2008).”
BackgroundMethodInfluential
A Role for Auditory Corticothalamic Feedback in the Perception of Complex Sounds
Homma, N. Y., Happel, M. F. K., Nodal, F. R., Ohl, F. W., King, A. J., & Bajo, V. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0397-17.2017 · Cited by 66 · see citing works
“Modulatory layer VI neurons form the majority of the projection from A1 to lemniscal thalamus (Nodal et al., 2006; Llano and Sherman, 2008).”
Background
Auditory tracts identified with combined fMRI and diffusion tractography
Javad, F., Warren, J. D., Micallef, C., Thornton, J. S., Golay, X., Yousry, T. A., & Mancini, L. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.09.007 · Cited by 65 · see citing works
“…projections are anatomically parallel to the ascending projections, but the corticocollicular projection bypasses theMGB on its way to the IC (Andersen et al., 1980; Brodal, 1981; Calford and Aitkin, 1983; Lee and Sherman, 2010; Llano and Sherman, 2008;Moller, 2006; Palmer and Rees, 2010).”
Background
Broca’s area – Thalamic connectivity
Bohsali, A. A., Triplett, W. T., Sudhyadhom, A., Gullett, J. M., McGregor, K., FitzGerald, D. B., Mareci, T. H., White, K. D., & Crosson, B. (2014) · Brain and Language · doi:10.1016/j.bandl.2014.12.001 · Cited by 64 · 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
“…and Linden, 2011; Hackett et al., 2011) and immunohistochemistry for the calcium binding proteins parvalbumin (PV) (Cruikshank et al., 2001; Llano and Sherman, 2008) and calbindin (CB) (Friauf, 1994; Cruikshank et al., 2001; Llano and Sherman, 2008; Lu et al., 2009) to identify the MGv and…”
BackgroundResultInfluential
Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections
Asilador, A. R., & Llano, D. A. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.615259 · Cited by 61 · see citing works
Self-citation
Auditory System
Malmierca, M. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00029-2 · Cited by 59 · see citing works
Induction of BDNF Expression in Layer II/III and Layer V Neurons of the Motor Cortex Is Essential for Motor Learning
Andreska, T., Rauskolb, S., Schukraft, N., Lüningschrör, P., Sasi, M., Signoret-Genest, J., Behringer, M., Blum, R., Sauer, M., Tovote, P., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0288-20.2020 · Cited by 58 · see citing works
“These neurons send dense afferents into the thalamus and are not involved in control of motor function (Deschenes et al., 1998; Llano and Sherman, 2008; Thomson, 2010; McKenna et al., 2011; Kim et al., 2014).”
Synaptic properties of the lemniscal and paralemniscal pathways to the mouse somatosensory thalamus
Mo, C., Petrof, I., Viaene, A. N., & Sherman, S. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1703222114 · Cited by 58 · see citing works
Self-citation
An Overview of Stimulus-Specific Adaptation in the Auditory Thalamus
Antunes, F. M., & Malmierca, M. S. (2013) · Brain Topography · doi:10.1007/s10548-013-0342-6 · Cited by 55 · see citing works
“3) (Bajo et al. 1995; Llano and Sherman 2008; Winer et al. 1999; Winer et al. 2001).”
Background
Different distributions of calbindin and calretinin immunostaining across the medial and dorsal divisions of the mouse medial geniculate body
Lu, C.-Y. E., Llano, D. A., & Sherman, S. M. (2009) · Hearing Research · doi:10.1016/j.heares.2009.07.009 · Cited by 56 · see citing works
“Although the current study did not examine tissue stained for both PV and either CR or CB, previous studies have shown a virtual absence of PV staining outside of the MGBv (Cruikshank et al., 2001; Llano and Sherman, 2008), and the current study shows a virtual absence of CB or CR staining within the MGBv.”
BackgroundResultInfluentialSelf-citation
Impact of peripheral hearing loss on top-down auditory processing
Lesicko, A. M. H., & Llano, D. A. (2016) · Hearing Research · doi:10.1016/j.heares.2016.05.018 · Cited by 54 · see citing works
“Projections from the cortex to subcortical structures (corticofugal projections), particularly to the thalamus and inferior colliculus, are numerous, heterogeneous and have substantial physiological impact on their target structures (Bajo and King, 2011; Bajo et al., 1995; He, 2003; Llano and Sherman, 2008; Ojima, 199…”
BackgroundSelf-citation
The Role of Cortico-Thalamo-Cortical Circuits in Language: Recurrent Circuits Revisited
Crosson, B. (2019) · Neuropsychology Review · doi:10.1007/s11065-019-09421-8 · Cited by 53 · see citing works
Presynaptic Neuronal Nicotinic Receptors Differentially Shape Select Inputs to Auditory Thalamus and Are Negatively Impacted by Aging
Sottile, S. Y., Hackett, T. A., Cai, R., Ling, L. L., Llano, D. A., & Caspary, D. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1795-17.2017 · Cited by 52 · see citing works
“Primary AC and vMGB are broadly reciprocally connected, with L6 corticothalamic terminals ending on distal, small-caliber, higher-order MGB dendrites (Bartlett et al., 2000; Winer et al., 2001; Smith et al., 2007; Llano and Sherman, 2008).”
BackgroundSelf-citation
From elementary synaptic circuits to information processing in primary auditory cortex
Wu, G. K., Tao, H. W., & Zhang, L. I. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.05.004 · Cited by 51 · see citing works
Evidence for layer-specific differences in auditory corticocollicular neurons
Slater, B. J., Willis, A. M., & Llano, D. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.053 · Cited by 50 · see citing works
“…5 and layer 6 neurons projecting to the thalamus have different intrinsic physiological and morphological properties, receive different local inputs, project to different parts of the thalamus and likely have different influences on the thalamus (Llano and Sherman, 2008, 2009; Theyel et al., 2010).”
Self-citation
Thalamic input to auditory cortex is locally heterogeneous but globally tonotopic
Vasquez-Lopez, S. A., Weissenberger, Y., Lohse, M., Keating, P., King, A. J., & Dahmen, J. C. (2017) · eLife · doi:10.7554/elife.25141 · Cited by 48 · see citing works
“While the study was designed to capture the 240 full extent of the thalamic input available to the auditory cortex, our own anatomical data together 241 with the work of others (Hackett et al., 2011; Llano and Sherman, 2008), show that the organization 242 we describe reflects almost exclusively the properties of the…”
BackgroundMethodInfluential
Anatomy of the auditory thalamocortical system in the mongolian gerbil: Nuclear origins and cortical field‐, layer‐, and frequency‐specificities
Saldeitis, K., Happel, M. F. K., Ohl, F. W., Scheich, H., & Budinger, E. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23540 · Cited by 48 · see citing works
“This is in general agreement with descriptions available from other species (rat: Kimura et al., 2003; Smith et al., 2012; mouse: Llano and Sherman, 2008; cat: Huang and Winer, 2000; monkey: Jones and Burton, 1976; Hashikawa et al., 1995).”
BackgroundResultInfluential
Layer 6b controls brain state via apical dendrites and the higher-order thalamocortical system
Zolnik, T. A., Bronec, A., Ross, A., Staab, M., Sachdev, R. N. S., Molnár, Z., Eickholt, B. J., & Larkum, M. E. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.021 · Cited by 51 · see citing works
Variation of connectivity across exemplar sensory and associative thalamocortical loops in the mouse
Mukherjee, A., Bajwa, N., Lam, N. H., Porrero, C., Clascá, F., & Halassa, M. M. (2020) · eLife · doi:10.7554/elife.62554 · Cited by 49 · see citing works
“…nucleus maybe explained by convergent cortical and/or subcortical inputs (Groh et al., 2014; Komura et al., 2013; Roth et al., 2016), indicating that at least some of these microcircuits may be performing computations on their inputs (Bieler et al., 2018; Mease et al., 2017; Whitmire et al., 2016).”
Background
Distinct anatomical connectivity patterns differentiate subdivisions of the nonlemniscal auditory thalamus in mice
Cai, D., Yue, Y., Su, X., Liu, M., Wang, Y., You, L., Xie, F., Deng, F., Chen, F., Luo, M., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy115 · Cited by 45 · see citing works
Subcortical syntax: Reconsidering the neural dynamics of language
Murphy, E., Hoshi, K., & Benítez‐Burraco, A. (2022) · Journal of Neurolinguistics · doi:10.1016/j.jneuroling.2022.101062 · Cited by 46 · see citing works
A comparative analysis of mouse and human medial geniculate nucleus connectivity: A DTI and anterograde tracing study
Keifer, O. P., Gutman, D. A., Hecht, E. E., Keilholz, S. D., & Ressler, K. J. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.047 · Cited by 44 · see citing works
“…the inferior colliculus to the auditory cortex (Budinger et al., 2000; Crippa et al., 2010; Geiser et al., 2012; Horie et al., 2013; Jones, 1985; Llano and Sherman, 2008; Mesulam and Pandya, 1973; Monakow, 1914; Poliak, 1926; Redies et al., 1989; Ryugo and Killackey, 1974; Tunturi, 1946;…”
Influential
Corticothalamic pathways from layer 5: emerging roles in computation and pathology
Mease, R. A., & Gonzalez, A. J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.730211 · Cited by 36 · see citing works
Dual compartments of the ventral division of the medial geniculate body projecting to the core region of the auditory cortex in C57BL/6 mice
Horie, M., Tsukano, H., Hishida, R., Takebayashi, H., & Shibuki, K. (2013) · Neuroscience Research · doi:10.1016/j.neures.2013.05.004 · Cited by 41 · see citing works
“However, it has recently been successively reported that very few neurons project to both AAF and AI (Lee et al., 2004a, 2004b; Llano and Sherman, 2008), and functional parallel processing has been assumed in the central nervous system of a cat (Davis et al., 1999; Ramachandran et al., 1999;…”
Background
Distribution of large terminal inputs from the primary and secondary somatosensory cortices to the dorsal thalamus in the rodent
Liao, C.-C., Chen, R.-F., Lai, W., Lin, R. C. S., & Yen, C. (2010) · The Journal of comparative neurology · doi:10.1002/cne.22354 · Cited by 37 · see citing works
“2608 The Journal of Comparative Neurology |Research in Systems Neuroscience the primary sensory cortical area was also reported for the auditory system (Llano and Sherman, 2008).”
Background
Synaptic Organization of Connections between the Temporal Cortex and Pulvinar Nucleus of the Tree Shrew
Chomsung, R. D., Wei, H., Day‐Brown, J. D., Petry, H. M., & Bickford, M. E. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp162 · Cited by 40 · see citing works
“Furthermore, the Pd and Pc form reciprocal connections with the temporal cortex, whereas higher order nuclei form nonreciprocal connections (Van Horn and Sherman 2004; Llano and Sherman 2008 ).”
Background
Neocortex
Kirkcaldie, M. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10004-4 · Cited by 40 · see citing works
Connectivity of the corticostriatal and thalamostriatal systems in normal and parkinsonian states: An update
Martel, A., & Galván, A. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105878 · Cited by 37 · see citing works
“Given that layer 6 is traditionally host to corticothalamic or corticocortical pyramidal cells (Chen et al., 2009; Llano and Sherman, 2008; Bourassa and Deschenes, 1995; Bourassa et al., 1995; Deschenes et al., 1998; Thomson, 2010), these results suggest that these corticostriatal pyramidal cells represent a newly des…”
Direct Relay Pathways from Lemniscal Auditory Thalamus to Secondary Auditory Field in Mice
Ohga, S., Tsukano, H., Horie, M., Terashima, H., Nishio, N., Kubota, Y., Takahashi, K., Hishida, R., Takebayashi, H., & Shibuki, K. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy234 · Cited by 35 · see citing works
Modulation of tonotopic ventral medial geniculate body is behaviorally relevant for speech recognition
Mihai, P. G., Moerel, M., Martino, F. D., Trampel, R., Kiebel, S. J., & von Kriegstein, K. (2019) · eLife · doi:10.7554/elife.44837 · Cited by 36 · see citing works
“…in A1 to the vMGB, but also from association cortices such as the motion sensitive part of the planum temporale (Tschentscher et al., 2019), may modulate information ascending through the lemniscal pathway, rather than convey information to the ventral division (Lee, 2013; Llano and Sherman, 2008).”
Pulvinar Modulates Contrast Responses in the Visual Cortex as a Function of Cortical Hierarchy
de Souza, B. O. F., Cortes, N., & Casanova, C. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz149 · Cited by 33 · 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
“Neurons in L6 of A1 project to the MGv and MGd, ending in small terminals on distal dendrites (Bajo et al. 1995; Bartlett et al. 2000; Llano and Sherman 2008; Ojima 1994; Rouiller and Welker 1991; Smith et al. 2007).”
Background
Massive multiplexing of spatially resolved single neuron projections with axonal BARseq
Yuan, L., Chen, X., Zhan, H., Henry, G. L., & Zador, A. M. (2024) · Nature Communications · doi:10.1038/s41467-024-52756-x · Cited by 30 · see citing works
“In contrast, CT neurons do not project to the tectum and mainly project to medial geniculate body (MG) in the thalamus 7,27 .”
Background
EphA Signaling Impacts Development of Topographic Connectivity in Auditory Corticofugal Systems
Torii, M., Hackett, T. A., RAKIC, P. T., Levitt, P. R., & Polley, D. B. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs066 · Cited by 30 · see citing works
“Similarly, gradients of EphA7-Fc and ephrin-A5 situ hybridization labeling within the MGB were quantified along the mediodorsal to ventrolateral axis through the MGB.”
Method
An auditory colliculothalamocortical brain slice preparation in mouse
Llano, D. A., Slater, B. J., Lesicko, A. M. H., & Stebbings, K. A. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00605.2013 · Cited by 27 · see citing works
Self-citation
Cortical layer 6 control of sensory responses in higher‐order thalamus
Ansorge, J., Humanes-Valera, D., Pauzin, F. P., Schwarz, M. K., & Krieger, P. (2020) · The Journal of Physiology · doi:10.1113/jp279915 · Cited by 29 · see citing works
“…can, however, increase whisker-evoked responses in cortex (Mease et al. 2016a; Zhang & Bruno, 2019) and in the visual and auditory cortico-thalamic loop layer 6 corticothalamic projections are largely to reciprocally connected thalamic regions (Van Horn & Sherman, 2004; Llano & Sherman, 2008).”
Background
Intracortical convergence of layer 6 neurons
Lee, C. C., Lam, Y., & Sherman, S. M. (2012) · Neuroreport · doi:10.1097/wnr.0b013e328356c1aa · Cited by 28 · see citing works
Self-citation
Learning-related population dynamics in the auditory thalamus
Gilad, A., Maor, I., & Mizrahi, A. (2020) · eLife · doi:10.7554/elife.56307 · Cited by 30 · see citing works
Experience-Dependent Coding of Time-Dependent Frequency Trajectories by Off Responses in Secondary Auditory Cortex
Chong, K. K., Anandakumar, D. B., Dunlap, A. G., Kacsoh, D. B., & Liu, R. C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2665-19.2020 · Cited by 25 · see citing works
“…though, since A2 receives input both from core auditory cortex (Covic and Sherman, 2011) as well as the dorsal division of the medial geniculate (Llano and Sherman, 2008), which exhibits traditional offset responses (He, 2001; Anderson and Linden, 2016), it remains to be seen whether the site…”
BackgroundResult
Organization of the Zone of Transition between the Pretectum and the Thalamus, with Emphasis on the Pretectothalamic Lamina
Legorreta, E. M., Horta‐Júnior, J. D. A. C., Berrebi, A. S., & Saldaña, E. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00082 · Cited by 25 · see citing works
“…la Mothe et al., 2006 [marmoset]; Anderson et al., 2007 [guinea pig]; Jones, 2007 [ferret, his Figure 11.4B; cynomolgus monkey, his Figures 11.8]; Llano and Sherman, 2008 [mouse]; Olkowicz et al., 2008 [opossum]; Wong et al., 2008 [squirrel]; Lu et al., 2009 [mouse]; Hardman and Ashwell, 2012…”
BackgroundInfluential
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
The subcortical auditory structures in the Mongolian gerbil: II. Frequency‐related topography of the connections with cortical field AI
Budinger, E., Brosch, M., Scheich, H., & Mylius, J. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23314 · Cited by 24 · see citing works
Multimodal cortical sensory pathways revealed by sequential transcranial electrical stimulation in mice
Hishida, R., Kudoh, M., & Shibuki, K. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.07.004 · Cited by 24 · see citing works
Biological constraints on stereotaxic targeting of functionally-defined cortical areas
Narayanan, D. P., Tsukano, H., Kline, A. M., Onodera, K., & Kato, H. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac275 · Cited by 23 · see citing works
“…area- targeted experiments, such as neural recording (Guo et al., 2012; Joachimsthaler et al., 2014; Siegle et al., 2021), connectivity tracing (Llano and Sherman, 2008; Oh et al., 2014; Schreiner and Winer, 2007; Wang and Burkhalter, 2007), and functional manipulation during behaviors…”
Background
Wiring of Divergent Networks in the Central Auditory System
Lee, C. C., Kishan, A. U., & Winer, J. A. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00046 · Cited by 23 · see citing works
“Two types of terminals arise from AI: small endings from thin axons of layer VI pyramidal neurons and large boutons from thick axons of layer V pyramidal neurons (Ojima, 1994; Winer et al., 1999; Llano and Sherman, 2008).”
Background
Lemniscal Corticothalamic Feedback in Auditory Scene Analysis
Homma, N. Y., & Bajo, V. M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.723893 · Cited by 23 · see citing works
Highly branched and complementary distributions of layer 5 and layer 6 auditory corticofugal axons in mouse
Issa, L. K., Sekaran, N. V. C., & Llano, D. A. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad227 · Cited by 23 · see citing works
Self-citation
The Role of Pulvinar in the Transmission of Information in the Visual Hierarchy
Cortes, N., & van Vreeswijk, C. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00029 · Cited by 23 · see citing works
“Nonreciprocal connections appear as a key component of higher-order thalamic nuclei (Sherman, 2007; Llano and Sherman, 2008; Theyel et al., 2010).”
Background
Presence of a Chaotic Region at the Sleep-Wake Transition in a Simplified Thalamocortical Circuit Model
Paul, K., Cauller, L. J., & Llano, D. A. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00091 · Cited by 22 · see citing works
“Corticothalamic projections, which arise from layers 5 to 6, terminate on TC neurons as well as on neurons of the RE (Liu and Jones, 1999; Zikopoulos and Barbas, 2006; Llano and Sherman, 2008).”
BackgroundInfluentialSelf-citation
Transthalamic Pathways for Cortical Function
Sherman, S. M., & Usrey, W. M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0909-24.2024 · Cited by 23 · see citing works
Self-citation
Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse
Patel, M. B., Sons, S. K., Yudintsev, G., Lesicko, A. M. H., Yang, L., Taha, G. A., Pierce, S. M., & Llano, D. A. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24106 · Cited by 21 · see citing works
“Although both structures receive inputs from AC (Andersen et al., 1980; Arnault and Roger, 1990; Salda~na et al., 1996; Llano and Sherman, 2008; Mellott et al., 2014), PP also receives a diverse set of other inputs from hypothalamus and visceral brainstem nuclei (Chiba and Murata, 1985; Risold et…”
BackgroundSelf-citation
Inhibitory synaptic mechanisms underlying functional diversity in auditory cortex
Zhang, L. I., Zhou, Y., & Tao, H. W. (2011) · The Journal of General Physiology · doi:10.1085/jgp.201110650 · Cited by 21 · see citing works
Patterns of Unilateral and Bilateral Projections From Layers 5 and 6 of the Auditory Cortex to the Inferior Colliculus in Mouse
Sekaran, N. V. C., Deshpande, M. S., Ibrahim, B. A., Xiao, G., Shinagawa, Y., & Llano, D. A. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.674098 · Cited by 20 · see citing works
“Parvalbumin (PV) immunostaining was done to delineate the borders of the lemniscal regions of the AC [primary AC and anterior auditory ﬁeld (Molinari et al., 1995; Kosaki et al., 1997; Cruikshank et al., 2001; Llano and Sherman, 2008)].”
BackgroundSelf-citation
Corticothalamic gating of population auditory thalamocortical transmission in mouse
Ibrahim, B. A., Murphy, C. A., Muscioni, G., Taheri, A., Yudintsev, G., Kenyon, R. V., Berger-Wolf, T. Y., Banks, M. I., & Llano, D. A. (2021) · eLife · doi:10.7554/elife.56645 · Cited by 20 · see citing works
Self-citation
Evidence for Layer-Specific Connectional Heterogeneity in the Mouse Auditory Corticocollicular System
Yudintsev, G., Asilador, A. R., Sons, S. K., Sekaran, N. V. C., Coppinger, M. N., Nair, K., Prasad, M., Xiao, G., Ibrahim, B. A., Shinagawa, Y., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2624-20.2021 · Cited by 19 · see citing works
“Layer 5 and layer 6 corticocollicular projections have different termination patterns in the IC Layer 5 and layer 6 corticofugal neurons have differential patterns of projections in other descending systems such as the corticothalamic pathway (Llano and Sherman, 2008).”
BackgroundMethodInfluentialSelf-citation
Functioning of Circuits Connecting Thalamus and Cortex
Sherman, S. M. (2017) · Comprehensive physiology · doi:10.1002/j.2040-4603.2017.tb00758.x · Cited by 18 · see citing works
“In the auditory system, anatomical evidence exists that the dorsal division of the medial geniculate nucleus receives driver input from layer 5 of primary auditory cortex (96,113,114).”
Self-citation
Familiarity with social sounds alters c-Fos expression in auditory cortex and interacts with estradiol in locus coeruleus
Moreno, A., Gumaste, A., Adams, G. K., Chong, K. K., Nguyen, M., Shepard, K. N., & Liu, R. C. (2018) · Hearing Research · doi:10.1016/j.heares.2018.06.020 · Cited by 17 · see citing works
“2E), comparable to previous publications that also used bregma positions within this range (Llano and Sherman, 2008; Tsukano et al., 2015).”
BackgroundResult
Modulation of the Primary Auditory Thalamus When Recognizing Speech with Background Noise
Mihai, P. G., Tschentscher, N., & von Kriegstein, K. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2902-20.2021 · Cited by 19 · see citing works
“, 771 2019), may modulate information ascending through the lemniscal pathway, rather than 772 convey information to the vMGB (Llano and Sherman, 2008; Lee, 2013).”
Background
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6
Lee, C. C., & Imaizumi, K. (2013) · Neurophysiology · doi:10.1007/s11062-013-9385-2 · Cited by 17 · 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
The Thalamus and Language
Llano, D. A. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-407794-2.00009-2 · Cited by 16 · see citing works
Self-citation
Auditory System
Malmierca, M. S., & Ryugo, D. K. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10024-x · Cited by 17 · see citing works
Frequency selectivity of echo responses in the mouse primary auditory cortex
Wang, M., Li, R., Li, J., Zhang, J., Chen, X., Zeng, S., & Liao, X. (2018) · Scientific Reports · doi:10.1038/s41598-017-18465-w · Cited by 15 · 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

Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate nucleus
Smith, P. H., Uhlrich, D. J., Manning, K., & Banks, M. I. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22682 · Cited by 109 · see citing works
Thalamocortical afferents of Lorente de Nó: medial geniculate axons that project to primary auditory cortex have collateral branches to layer I
Cetas, J. S., de Venecia, R. K., & McMullen, N. T. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01355-4 · Cited by 42 · see citing works
Mouse auditory cortex sub-fields receive neuronal projections from MGB subdivisions independently
Wang, C., Jiang, Z.-Y., Chai, J., Chen, H.-S., Liu, L.-X., Dang, T., & Meng, X. (2024) · Scientific Reports · doi:10.1038/s41598-024-57815-3 · Cited by 2 · see citing works
Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: Study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body
Winer, J. A., & Larue, D. T. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902570212 · Cited by 161 · see citing works
Anatomy of the auditory thalamocortical system in the mongolian gerbil: Nuclear origins and cortical field‐, layer‐, and frequency‐specificities
Saldeitis, K., Happel, M. F. K., Ohl, F. W., Scheich, H., & Budinger, E. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23540 · Cited by 48 · see citing works

Authors: Llano, D. A., & Sherman, S. M.
Affiliations: University of Chicago (US)
Corresponding author: Llano, Daniel A.
ORCID: Llano, Daniel A.
Sherman, S. Murray
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 2008-01-07
Volume: 507
Issue: 2
Pages: 1209-1227
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.21602
OpenAlex: W2007541448
Cited by: 186
References: 105
Citations by year: 2026: 6 · 2025: 8 · 2024: 4 · 2023: 11 · 2022: 7 · 2021: 30 · 2020: 14 · 2019: 12 · 2018: 10 · 2017: 10 · 2016: 14 · 2015: 8 · 2014: 9 · 2013: 9 · 2012: 7
FWCI: 4.65
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: University of Chicago
National Eye Institute (R01EY003038, EY003038)
National Institute on Deafness and Other Communication Disorders (R01DC008794, DC008320, DC-008794, K08DC008320)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: auditory thalamus, corticothalamic projections, thalamocortical connections, medial geniculate body, auditory cortex, primary auditory cortex, anterior auditory field, layer 5 neurons, retrograde tracing, anterograde tracing, cortical columns, mice
MeSH terms: Animals, Auditory Cortex, Auditory Pathways, Auditory Perception, Axons, Biotin, Brain Mapping, Calcium-Binding Proteins, Electron Transport Complex IV, Dextrans, Efferent Pathways, Female, Geniculate Bodies, Immunohistochemistry, Interneurons, Male, Mice, Inbred BALB C, Staining and Labeling, Biomarkers, Presynaptic Terminals, Pyramidal Cells, Mice

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Evidence for nonreciprocal organization of the mouse auditory thalamocortical‐corticothalamic projection systems

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