Parallel Pathways for Sound Processing and Functional Connectivity Among Layer 5 and 6 Auditory Corticofugal Neurons

Overview

Journal Elife

Specialty Biology

Date 2019 Feb 9

PMID 30735128

Citations 52

Authors

Ross S Williamson

Daniel B Polley

Affiliations

Soon will be listed here.

Abstract

Cortical layers (L) 5 and 6 are populated by intermingled cell-types with distinct inputs and downstream targets. Here, we made optogenetically guided recordings from L5 corticofugal (CF) and L6 corticothalamic (CT) neurons in the auditory cortex of awake mice to discern differences in sensory processing and underlying patterns of functional connectivity. Whereas L5 CF neurons showed broad stimulus selectivity with sluggish response latencies and extended temporal non-linearities, L6 CTs exhibited sparse selectivity and rapid temporal processing. L5 CF spikes lagged behind neighboring units and imposed weak feedforward excitation within the local column. By contrast, L6 CT spikes drove robust and sustained activity, particularly in local fast-spiking interneurons. Our findings underscore a duality among sub-cortical projection neurons, where L5 CF units are canonical broadcast neurons that integrate sensory inputs for transmission to distributed downstream targets, while L6 CT neurons are positioned to regulate thalamocortical response gain and selectivity.

Citing Articles

FOXP2-immunoreactive corticothalamic neurons in neocortical layers 6a and 6b are tightly regulated by neuromodulatory systems.

Qi G, Yang D, Messore F, Bast A, Yanez F, Oberlaender M iScience. 2025; 28(1):111646.

PMID: 39868047 PMC: 11758397. DOI: 10.1016/j.isci.2024.111646.

Noncanonical Short-Latency Auditory Pathway Directly Activates Deep Cortical Layers.

Garcia M, Kline A, Onodera K, Tsukano H, Dandu P, Acosta H bioRxiv. 2025; .

PMID: 39829930 PMC: 11741258. DOI: 10.1101/2025.01.06.631598.

Neural Correlates of Perceptual Plasticity in the Auditory Midbrain and Thalamus.

Ying R, Stolzberg D, Caras M J Neurosci. 2025; 45(10).

PMID: 39753303 PMC: 11884394. DOI: 10.1523/JNEUROSCI.0691-24.2024.

Convolutional neural network models describe the encoding subspace of local circuits in auditory cortex.

Wingert J, Parida S, Norman-Haignere S, David S bioRxiv. 2024; .

PMID: 39574636 PMC: 11581007. DOI: 10.1101/2024.11.07.622384.

Cell-type-specific enhancement of deviance detection by synaptic zinc in the mouse auditory cortex.

McCollum M, Manning A, Bender P, Mendelson B, Anderson C Proc Natl Acad Sci U S A. 2024; 121(40):e2405615121.

PMID: 39312661 PMC: 11459170. DOI: 10.1073/pnas.2405615121.

References

Rockland K . Convergence and branching patterns of round, type 2 corticopulvinar axons. J Comp Neurol. 1998; 390(4):515-36. DOI: 10.1002/(sici)1096-9861(19980126)390:4<515::aid-cne5>3.0.co;2-3. View

Bourassa J, Pinault D, Deschenes M . Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur J Neurosci. 1995; 7(1):19-30. DOI: 10.1111/j.1460-9568.1995.tb01016.x. View

Yu Y, Xiong Y, Chan Y, He J . Corticofugal gating of auditory information in the thalamus: an in vivo intracellular recording study. J Neurosci. 2004; 24(12):3060-9. PMC: 6729842. DOI: 10.1523/JNEUROSCI.4897-03.2004. View

Bajo V, Rouiller E, Welker E, Clarke S, Villa A, De Ribaupierre Y . Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex. Hear Res. 1995; 83(1-2):161-74. DOI: 10.1016/0378-5955(94)00199-z. View

Sherman S, Guillery R . Distinct functions for direct and transthalamic corticocortical connections. J Neurophysiol. 2011; 106(3):1068-77. DOI: 10.1152/jn.00429.2011. View

Li N, Chen T, Guo Z, Gerfen C, Svoboda K . A motor cortex circuit for motor planning and movement. Nature. 2015; 519(7541):51-6. DOI: 10.1038/nature14178. View

Sundberg S, Granseth B . Cre-expressing neurons in the cortical white matter of Ntsr1-Cre GN220 mice. Neurosci Lett. 2018; 675:36-40. DOI: 10.1016/j.neulet.2018.03.053. View

Moriizumi T, Hattori T . Pyramidal cells in rat temporoauditory cortex project to both striatum and inferior colliculus. Brain Res Bull. 1991; 27(1):141-4. DOI: 10.1016/0361-9230(91)90297-w. View

Agmon A, Connors B . Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci. 1992; 12(1):319-29. PMC: 6575688. View

10.

Harris K, Mrsic-Flogel T . Cortical connectivity and sensory coding. Nature. 2013; 503(7474):51-8. DOI: 10.1038/nature12654. View

11.

Bartlett E, Stark J, Guillery R, Smith P . Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience. 2000; 100(4):811-28. DOI: 10.1016/s0306-4522(00)00340-7. View

12.

Veinante P, Lavallee P, Deschenes M . Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat. J Comp Neurol. 2000; 424(2):197-204. DOI: 10.1002/1096-9861(20000821)424:2<197::aid-cne1>3.0.co;2-6. View

13.

McCormick D, Connors B, Lighthall J, Prince D . Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985; 54(4):782-806. DOI: 10.1152/jn.1985.54.4.782. View

14.

Connors B, Gutnick M, Prince D . Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol. 1982; 48(6):1302-20. DOI: 10.1152/jn.1982.48.6.1302. View

15.

Ahrens M, Linden J, Sahani M . Nonlinearities and contextual influences in auditory cortical responses modeled with multilinear spectrotemporal methods. J Neurosci. 2008; 28(8):1929-42. PMC: 6671443. DOI: 10.1523/JNEUROSCI.3377-07.2008. View

16.

Wehr M, Zador A . Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron. 2005; 47(3):437-45. DOI: 10.1016/j.neuron.2005.06.009. View

17.

Constantinople C, Bruno R . Deep cortical layers are activated directly by thalamus. Science. 2013; 340(6140):1591-4. PMC: 4203320. DOI: 10.1126/science.1236425. View

18.

Deschenes M, Bourassa J, Pinault D . Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 1994; 664(1-2):215-9. DOI: 10.1016/0006-8993(94)91974-7. View

19.

Xiong X, Liang F, Zingg B, Ji X, Ibrahim L, Tao H . Auditory cortex controls sound-driven innate defense behaviour through corticofugal projections to inferior colliculus. Nat Commun. 2015; 6:7224. PMC: 4467028. DOI: 10.1038/ncomms8224. View

20.

Harris K, Shepherd G . The neocortical circuit: themes and variations. Nat Neurosci. 2015; 18(2):170-81. PMC: 4889215. DOI: 10.1038/nn.3917. View