Gain control by layer six in cortical circuits of vision

Gain control by layer six in cortical circuits of vision

Play all audios:

Loading...

ABSTRACT After entering the cerebral cortex, sensory information spreads through six different horizontal neuronal layers that are interconnected by vertical axonal projections. It is


believed that through these projections layers can influence each other's response to sensory stimuli, but the specific role that each layer has in cortical processing is still poorly


understood. Here we show that layer six in the primary visual cortex of the mouse has a crucial role in controlling the gain of visually evoked activity in neurons of the upper layers


without changing their tuning to orientation. This gain modulation results from the coordinated action of layer six intracortical projections to superficial layers and deep projections to


the thalamus, with a substantial role of the intracortical circuit. This study establishes layer six as a major mediator of cortical gain modulation and suggests that it could be a node


through which convergent inputs from several brain areas can regulate the earliest steps of cortical visual processing. Access through your institution Buy or subscribe This is a preview of


subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 51 print issues and online access $199.00 per year only


$3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout


ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS LATERAL INHIBITION IN V1


CONTROLS NEURAL AND PERCEPTUAL CONTRAST SENSITIVITY Article 03 March 2025 ON/OFF DOMAINS SHAPE RECEPTIVE FIELD STRUCTURE IN MOUSE VISUAL CORTEX Article Open access 05 May 2022 LAMINAR


COMPARTMENTALIZATION OF ATTENTION MODULATION IN AREA V4 ALIGNS WITH THE DEMANDS OF VISUAL PROCESSING HIERARCHY IN THE CORTEX Article Open access 09 November 2023 REFERENCES * Lorente de No,


R. in _Physiology of the Nervous System_ (ed. Fulton, J.F. ) 274–301 (Oxford Univ. Press, 1943) Google Scholar  * Douglas, R. J. & Martin, K. A. Neuronal circuits of the neocortex.


_Annu. Rev. Neurosci._ 27, 419–451 (2004) Article  CAS  PubMed  Google Scholar  * Lefort, S., Tomm, C., Floyd Sarria, J. C. & Petersen, C. C. The excitatory neuronal network of the C2


barrel column in mouse primary somatosensory cortex. _Neuron_ 61, 301–316 (2009) Article  CAS  PubMed  Google Scholar  * Thomson, A. M. & Bannister, A. P. Interlaminar connections in the


neocortex. _Cereb. Cortex_ 13, 5–14 (2003) Article  PubMed  Google Scholar  * Callaway, E. M. Local circuits in primary visual cortex of the macaque monkey. _Annu. Rev. Neurosci._ 21, 47–74


(1998) Article  CAS  PubMed  Google Scholar  * Dantzker, J. L. & Callaway, E. M. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. _Nature


Neurosci._ 3, 701–707 (2000) Article  CAS  PubMed  Google Scholar  * Thomson, A. M. Neocortical layer 6, a review. _Front. Neuroanat._ 4, 13 (2010) PubMed  PubMed Central  Google Scholar  *


Bourassa, J. & Deschenes, M. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. _Neuroscience_ 66, 253–263


(1995) Article  CAS  PubMed  Google Scholar  * Binzegger, T., Douglas, R. J. & Martin, K. A. Stereotypical bouton clustering of individual neurons in cat primary visual cortex. _J.


Neurosci._ 27, 12242–12254 (2007) Article  CAS  PubMed  PubMed Central  Google Scholar  * Zhang, Z. W. & Deschenes, M. Intracortical axonal projections of lamina VI cells of the primary


somatosensory cortex in the rat: a single-cell labeling study. _J. Neurosci._ 17, 6365–6379 (1997) Article  CAS  PubMed  PubMed Central  Google Scholar  * Jones, E. G. _The_ _Thalamus_


(Cambridge Univ. Press, 2007) Google Scholar  * Guillery, R. W. & Sherman, S. M. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual


system. _Neuron_ 33, 163–175 (2002) Article  CAS  PubMed  Google Scholar  * Sillito, A. M. & Jones, H. E. Corticothalamic interactions in the transfer of visual information. _Phil.


Trans. R. Soc. Lond. B_ 357, 1739–1752 (2002) Article  Google Scholar  * Briggs, F. & Usrey, W. M. Emerging views of corticothalamic function. _Curr. Opin. Neurobiol._ 18, 403–407 (2008)


Article  CAS  PubMed  PubMed Central  Google Scholar  * Cudeiro, J. & Sillito, A. M. Looking back: corticothalamic feedback and early visual processing. _Trends Neurosci._ 29, 298–306


(2006) Article  CAS  PubMed  Google Scholar  * Sillito, A. M., Cudeiro, J. & Jones, H. E. Always returning: feedback and sensory processing in visual cortex and thalamus. _Trends


Neurosci._ 29, 307–316 (2006) Article  CAS  PubMed  Google Scholar  * Bolz, J. & Gilbert, C. D. Generation of end-inhibition in the visual cortex via interlaminar connections. _Nature_


320, 362–365 (1986) Article  ADS  CAS  PubMed  Google Scholar  * Grieve, K. L. & Sillito, A. M. A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical


end inhibition. _Exp. Brain Res._ 87, 521–529 (1991) Article  CAS  PubMed  Google Scholar  * Gong, S. et al. Targeting Cre recombinase to specific neuron populations with bacterial


artificial chromosome constructs. _J. Neurosci._ 27, 9817–9823 (2007) Article  CAS  PubMed  PubMed Central  Google Scholar  * Nagel, G. et al. Channelrhodopsin-2, a directly light-gated


cation-selective membrane channel. _Proc. Natl Acad. Sci. USA_ 100, 13940–13945 (2003) Article  ADS  CAS  PubMed  PubMed Central  Google Scholar  * Boyden, E. S., Zhang, F., Bamberg, E.,


Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. _Nature Neurosci._ 8, 1263–1268 (2005) Article  CAS  PubMed  Google Scholar  *


Niell, C. M. & Stryker, M. P. Highly selective receptive fields in mouse visual cortex. _J. Neurosci._ 28, 7520–7536 (2008) Article  CAS  PubMed  PubMed Central  Google Scholar  * Hubel,


D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. _J. Physiol._ 160, 106–154 (1962) Article  CAS  PubMed  PubMed


Central  Google Scholar  * Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. _Nature_ 463, 98–102 (2010) Article  ADS  CAS 


PubMed  PubMed Central  Google Scholar  * Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. _Cell_ 141, 154–165 (2010) Article  CAS  PubMed


  PubMed Central  Google Scholar  * Rafols, J. A. & Valverde, F. The structure of the dorsal lateral geniculate nucleus in the mouse. A Golgi and electron microscopic study. _J. Comp.


Neurol._ 150, 303–331 (1973) Article  CAS  PubMed  Google Scholar  * Salinas, E. & Thier, P. Gain modulation: a major computational principle of the central nervous system. _Neuron_ 27,


15–21 (2000) Article  CAS  PubMed  Google Scholar  * Brotchie, P. R., Andersen, R. A., Snyder, L. H. & Goodman, S. J. Head position signals used by parietal neurons to encode locations


of visual stimuli. _Nature_ 375, 232–235 (1995) Article  ADS  CAS  PubMed  Google Scholar  * Treue, S. & Martinez Trujillo, J. C. Feature-based attention influences motion processing


gain in macaque visual cortex. _Nature_ 399, 575–579 (1999) Article  ADS  CAS  PubMed  Google Scholar  * McAdams, C. J. & Maunsell, J. H. Effects of attention on orientation-tuning


functions of single neurons in macaque cortical area V4. _J. Neurosci._ 19, 431–441 (1999) Article  CAS  PubMed  PubMed Central  Google Scholar  * Silver, R. A., Lubke, J., Sakmann, B. &


Feldmeyer, D. High-probability uniquantal transmission at excitatory synapses in barrel cortex. _Science_ 302, 1981–1984 (2003) Article  ADS  CAS  PubMed  Google Scholar  * Adesnik, H.


& Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. _Nature_ 464, 1155–1160 (2010) Article  ADS  CAS  PubMed  PubMed Central  Google Scholar  *


Markram, H. et al. Interneurons of the neocortical inhibitory system. _Nature Rev. Neurosci._ 5, 793–807 (2004) Article  CAS  Google Scholar  * Ascoli, G. A. et al. Petilla terminology:


nomenclature of features of GABAergic interneurons of the cerebral cortex. _Nature Rev. Neurosci._ 9, 557–568 (2008) Article  CAS  Google Scholar  * Chance, F. S., Abbott, L. F. & Reyes,


A. D. Gain modulation from background synaptic input. _Neuron_ 35, 773–782 (2002) Article  CAS  PubMed  Google Scholar  * Shadlen, M. N. & Newsome, W. T. The variable discharge of


cortical neurons: implications for connectivity, computation, and information coding. _J. Neurosci._ 18, 3870–3896 (1998) Article  CAS  PubMed  PubMed Central  Google Scholar  * Murphy, B.


K. & Miller, K. D. Multiplicative gain changes are induced by excitation or inhibition alone. _J. Neurosci._ 23, 10040–10051 (2003) Article  CAS  PubMed  PubMed Central  Google Scholar 


* Andolina, I. M., Jones, H. E., Wang, W. & Sillito, A. M. Corticothalamic feedback enhances stimulus response precision in the visual system. _Proc. Natl Acad. Sci. USA_ 104, 1685–1690


(2007) Article  ADS  CAS  PubMed  PubMed Central  Google Scholar  * Wang, W., Jones, H. E., Andolina, I. M., Salt, T. E. & Sillito, A. M. Functional alignment of feedback effects from


visual cortex to thalamus. _Nature Neurosci._ 9, 1330–1336 (2006) Article  CAS  PubMed  Google Scholar  * Wörgotter, F., Nelle, E., Li, B. & Funke, K. The influence of corticofugal


feedback on the temporal structure of visual responses of cat thalamic relay cells. _J. Physiol._ 509, 797–815 (1998) Article  PubMed  PubMed Central  Google Scholar  * McClurkin, J. W.


& Marrocco, R. T. Visual cortical input alters spatial tuning in monkey lateral geniculate nucleus cells. _J. Physiol._ 348, 135–152 (1984) Article  CAS  PubMed  PubMed Central  Google


Scholar  * Murphy, P. C., Duckett, S. G. & Sillito, A. M. Feedback connections to the lateral geniculate nucleus and cortical response properties. _Science_ 286, 1552–1554 (1999) Article


  CAS  PubMed  Google Scholar  * Casagrande, V. A. & Kaas, J. H. _The Afferent, Iintrinsic and Efferent Connections of Primary Visual Cortex in Primates_ (eds Peters, A. & Rockland,


P. ) (Plenum, 1994) Google Scholar  * Grubb, M. S. & Thompson, I. D. Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. _J.


Neurophysiol._ 90, 3594–3607 (2003) Article  PubMed  Google Scholar  * Brainard, D. H. The psychophysics toolbox. _Spat. Vis._ 10, 433–436 (1997) Article  CAS  PubMed  Google Scholar  * Fee,


M. S., Mitra, P. P. & Kleinfeld, D. Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. _J. Neurosci. Methods_ 69, 175–188


(1996) Article  CAS  PubMed  Google Scholar  * Kerlin, A. M., Andermann, M. L., Berezovskii, V. K. & Reid, R. C. Broadly tuned response properties of diverse inhibitory neuron subtypes


in mouse visual cortex. _Neuron_ 67, 858–871 (2010) Article  CAS  PubMed  PubMed Central  Google Scholar  * Ringach, D. L., Shapley, R. M. & Hawken, M. J. Orientation selectivity in


macaque V1: diversity and laminar dependence. _J. Neurosci._ 22, 5639–5651 (2002) Article  CAS  PubMed  PubMed Central  Google Scholar  * Bortone, D. & Polleux, F. KCC2 expression


promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. _Neuron_ 62, 53–71 (2009) Article  CAS  PubMed  PubMed Central  Google Scholar  *


Bagnall, M. W., Hull, C., Bushong, E. A., Ellisman, M. H. & Scanziani, M. Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure


reliable transmission. _Neuron_ 71, 180–194 (2011) Article  CAS  PubMed  PubMed Central  Google Scholar  Download references ACKNOWLEDGEMENTS We are grateful to M. Carandini, J. Isaacson and


the members of the Scanziani and Isaacson laboratories for helpful discussions of this project, to J. Isaacson, R. Malinow and T. Komiyama for providing feedback on the manuscript, to P.


Abelkop for histological help and neonatal viral injections, to J. Evora for mouse colony support and genotyping, to B. Atallah for sharing the technique for silencing the cortex by


photostimulation of parvalbumin neurons and for help with the _in vivo_ recording setup and to W. Bruns for help coding analysis software. We thank the UCSD Neuroscience Microscopy Facility


(P30 NS047101) for the use of their imaging equipment. S.R.O. and H.A. were supported by postdoctoral fellowships from the Helen Hay Whitney Foundation. D.S.B was supported by a UCSD


Neurobiology Training Grant (NINDS: 5T32NS007220-28). M.S. is an investigator of the Howard Hughes Medical Institute. This work was also supported National Institutes of Health grant RO1


NS069010 and by the Gatsby Charitable Foundation. AUTHOR INFORMATION Author notes * Shawn R. Olsen and Dante S. Bortone: These authors contributed equally to this work. AUTHORS AND


AFFILIATIONS * Neurobiology Section and Department of Neuroscience, Howard Hughes Medical Institute, Center for Neural Circuits and Behavior, University of California San Diego, La Jolla,


92093-0634, California, USA Shawn R. Olsen, Dante S. Bortone, Hillel Adesnik & Massimo Scanziani Authors * Shawn R. Olsen View author publications You can also search for this author


inPubMed Google Scholar * Dante S. Bortone View author publications You can also search for this author inPubMed Google Scholar * Hillel Adesnik View author publications You can also search


for this author inPubMed Google Scholar * Massimo Scanziani View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS H.A. performed the initial


physiological characterization of the NTSR1-Cre expression system with optogenetic tools. H.A. also developed the _in vivo_ awake recording preparation on the treadmill. S.R.O. performed all


_in vivo_ recordings. D.S.B. performed all _in vitro_ recordings and anatomical reconstructions. S.R.O. and M.S. designed the study. M.S. wrote the paper. CORRESPONDING AUTHORS


Correspondence to Shawn R. Olsen or Massimo Scanziani. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. SUPPLEMENTARY INFORMATION SUPPLEMENTARY


FIGURES This file contains Supplementary Figures 1-10 with legends. (PDF 19395 kb) POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3


POWERPOINT SLIDE FOR FIG. 4 POWERPOINT SLIDE FOR FIG. 5 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Olsen, S., Bortone, D., Adesnik, H. _et al._ Gain


control by layer six in cortical circuits of vision. _Nature_ 483, 47–52 (2012). https://doi.org/10.1038/nature10835 Download citation * Received: 29 August 2011 * Accepted: 04 January 2012


* Published: 22 February 2012 * Issue Date: 01 March 2012 * DOI: https://doi.org/10.1038/nature10835 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this


content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative