Top-Down-Mediated Facilitation in the Visual Cortex Is Gated by Subcortical Neuromodulation

Overview

Journal J Neurosci

Specialty Neurology

Date 2016 Mar 11

PMID 26961946

Citations 25

Authors

Diego E Pafundo

Mark A Nicholas

Ruilin Zhang

Sandra J Kuhlman

Affiliations

Soon will be listed here.

Abstract

Response properties in primary sensory cortices are highly dependent on behavioral state. For example, the nucleus basalis of the forebrain plays a critical role in enhancing response properties of excitatory neurons in primary visual cortex (V1) during active exploration and learning. Given the strong reciprocal connections between hierarchically arranged cortical regions, how are increases in sensory response gain constrained to prevent runaway excitation? To explore this, we used in vivo two-photon guided cell-attached recording in conjunction with spatially restricted optogenetic photo-inhibition of higher-order visual cortex in mice. We found that the principle feedback projection to V1 originating from the lateral medial area (LM) facilitated visual responses in layer 2/3 excitatory neurons by ∼20%. This facilitation was reduced by half during basal forebrain activation due to differential response properties between LM and V1. Our results demonstrate that basal-forebrain-mediated increases in response gain are localized to V1 and are not propagated to LM and establish that subcortical modulation of visual cortex is regionally distinct.

Citing Articles

Cholinergic input to mouse visual cortex signals a movement state and acutely enhances layer 5 responsiveness.

Yogesh B, Keller G Elife. 2024; 12.

PMID: 39057843 PMC: 11281783. DOI: 10.7554/eLife.89986.

How 'visual' is the visual cortex? The interactions between the visual cortex and other sensory, motivational and motor systems as enabling factors for visual perception.

Pennartz C, Oude Lohuis M, Olcese U Philos Trans R Soc Lond B Biol Sci. 2023; 378(1886):20220336.

PMID: 37545313 PMC: 10404929. DOI: 10.1098/rstb.2022.0336.

Visual experience has opposing influences on the quality of stimulus representation in adult primary visual cortex.

Jeon B, Fuchs T, Chase S, Kuhlman S Elife. 2022; 11.

PMID: 36321876 PMC: 9629826. DOI: 10.7554/eLife.80361.

Selective enhancement of neural coding in V1 underlies fine-discrimination learning in tree shrew.

Schumacher J, McCann M, Maximov K, Fitzpatrick D Curr Biol. 2022; 32(15):3245-3260.e5.

PMID: 35767997 PMC: 9378627. DOI: 10.1016/j.cub.2022.06.009.

Existing function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task.

Jeon B, Fuchs T, Chase S, Kuhlman S Nat Commun. 2022; 13(1):3638.

PMID: 35752622 PMC: 9233699. DOI: 10.1038/s41467-022-31440-y.

References

Carcea I, Froemke R . Cortical plasticity, excitatory-inhibitory balance, and sensory perception. Prog Brain Res. 2013; 207:65-90. PMC: 4300113. DOI: 10.1016/B978-0-444-63327-9.00003-5. View

Goard M, Dan Y . Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci. 2009; 12(11):1444-9. PMC: 3576925. DOI: 10.1038/nn.2402. View

Yang W, Carrasquillo Y, Hooks B, Nerbonne J, Burkhalter A . Distinct balance of excitation and inhibition in an interareal feedforward and feedback circuit of mouse visual cortex. J Neurosci. 2013; 33(44):17373-84. PMC: 3812505. DOI: 10.1523/JNEUROSCI.2515-13.2013. View

Fu Y, Tucciarone J, Espinosa J, Sheng N, Darcy D, Nicoll R . A cortical circuit for gain control by behavioral state. Cell. 2014; 156(6):1139-1152. PMC: 4041382. DOI: 10.1016/j.cell.2014.01.050. View

Pinto L, Goard M, Estandian D, Xu M, Kwan A, Lee S . Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci. 2013; 16(12):1857-1863. PMC: 4201942. DOI: 10.1038/nn.3552. View

Munoz W, Rudy B . Spatiotemporal specificity in cholinergic control of neocortical function. Curr Opin Neurobiol. 2014; 26:149-60. PMC: 4100208. DOI: 10.1016/j.conb.2014.02.015. View

Nassi J, Gomez-Laberge C, Kreiman G, Born R . Corticocortical feedback increases the spatial extent of normalization. Front Syst Neurosci. 2014; 8:105. PMC: 4039070. DOI: 10.3389/fnsys.2014.00105. View

Kuhlman S, Huang Z . High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLoS One. 2008; 3(4):e2005. PMC: 2289876. DOI: 10.1371/journal.pone.0002005. View

de Pasquale R, Sherman S . A modulatory effect of the feedback from higher visual areas to V1 in the mouse. J Neurophysiol. 2013; 109(10):2618-31. PMC: 3653048. DOI: 10.1152/jn.01083.2012. View

10.

Guo Z, Li N, Huber D, Ophir E, Gutnisky D, Ting J . Flow of cortical activity underlying a tactile decision in mice. Neuron. 2013; 81(1):179-94. PMC: 3984938. DOI: 10.1016/j.neuron.2013.10.020. View

11.

Henny P, Jones B . Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci. 2008; 27(3):654-70. PMC: 2426826. DOI: 10.1111/j.1460-9568.2008.06029.x. View

12.

Ji W, Gamanut R, Bista P, DSouza R, Wang Q, Burkhalter A . Modularity in the Organization of Mouse Primary Visual Cortex. Neuron. 2015; 87(3):632-43. PMC: 4529541. DOI: 10.1016/j.neuron.2015.07.004. View

13.

Li Y, Ibrahim L, Liu B, Zhang L, Tao H . Linear transformation of thalamocortical input by intracortical excitation. Nat Neurosci. 2013; 16(9):1324-30. PMC: 3855439. DOI: 10.1038/nn.3494. View

14.

Bigl V, Woolf N, Butcher L . Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull. 1982; 8(6):727-49. DOI: 10.1016/0361-9230(82)90101-0. View

15.

Marshel J, Garrett M, Nauhaus I, Callaway E . Functional specialization of seven mouse visual cortical areas. Neuron. 2011; 72(6):1040-54. PMC: 3248795. DOI: 10.1016/j.neuron.2011.12.004. View

16.

Wang Q, Burkhalter A . Area map of mouse visual cortex. J Comp Neurol. 2007; 502(3):339-57. DOI: 10.1002/cne.21286. View

17.

Lecoq J, Savall J, Vucinic D, Grewe B, Kim H, Li J . Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging. Nat Neurosci. 2014; 17(12):1825-9. PMC: 5289313. DOI: 10.1038/nn.3867. View

18.

Gilbert C, Li W . Top-down influences on visual processing. Nat Rev Neurosci. 2013; 14(5):350-63. PMC: 3864796. DOI: 10.1038/nrn3476. View

19.

Wang Q, Sporns O, Burkhalter A . Network analysis of corticocortical connections reveals ventral and dorsal processing streams in mouse visual cortex. J Neurosci. 2012; 32(13):4386-99. PMC: 3328193. DOI: 10.1523/JNEUROSCI.6063-11.2012. View

20.

Hasselmo M, Sarter M . Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology. 2010; 36(1):52-73. PMC: 2992803. DOI: 10.1038/npp.2010.104. View