The Effects of Arousal on Apical Amplification and Conscious State

Overview

Journal Neurosci Conscious

Publisher Oxford University Press

Date 2018 Jun 8

PMID 29877512

Citations 22

Authors

W A Phillips

M E Larkum

C W Harley

S M Silverstein

Affiliations

Soon will be listed here.

Abstract

Neocortical pyramidal cells can integrate two classes of input separately and use one to modulate response to the other. Their tuft dendrites are electrotonically separated from basal dendrites and soma by the apical dendrite, and apical hyperpolarization-activated currents (I) further isolate subthreshold integration of tuft inputs. When apical depolarization exceeds a threshold, however, it can enhance response to the basal inputs that specify the cell's selective sensitivity. This process is referred to as apical amplification (AA). We review evidence suggesting that, by regulating I in the apical compartments, adrenergic arousal controls the coupling between apical and somatic integration zones thus modifying cognitive capabilities closely associated with consciousness. Evidence relating AA to schizophrenia, sleep, and anesthesia is reviewed, and we assess theories that emphasize the relevance of AA to consciousness. Implications for theories of neocortical computation that emphasize context-sensitive modulation are summarized. We conclude that the findings concerning AA and its regulation by arousal offer a new perspective on states of consciousness, the function and evolution of neocortex, and psychopathology. Many issues worthy of closer examination arise.

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References

Oizumi M, Albantakis L, Tononi G . From the phenomenology to the mechanisms of consciousness: Integrated Information Theory 3.0. PLoS Comput Biol. 2014; 10(5):e1003588. PMC: 4014402. DOI: 10.1371/journal.pcbi.1003588. View

Huang S, Trevino M, He K, Ardiles A, de Pasquale R, Guo Y . Pull-push neuromodulation of LTP and LTD enables bidirectional experience-induced synaptic scaling in visual cortex. Neuron. 2012; 73(3):497-510. PMC: 3373163. DOI: 10.1016/j.neuron.2011.11.023. View

Lamme V, Roelfsema P . The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 2000; 23(11):571-9. DOI: 10.1016/s0166-2236(00)01657-x. View

Hohwy J . The neural correlates of consciousness: new experimental approaches needed?. Conscious Cogn. 2009; 18(2):428-38. DOI: 10.1016/j.concog.2009.02.006. View

Cannon T, Hennah W, van Erp T, Thompson P, Lonnqvist J, Huttunen M . Association of DISC1/TRAX haplotypes with schizophrenia, reduced prefrontal gray matter, and impaired short- and long-term memory. Arch Gen Psychiatry. 2005; 62(11):1205-13. DOI: 10.1001/archpsyc.62.11.1205. View

Torniainen M, Suvisaari J, Partonen T, E Castaneda A, Kuha A, Suokas J . Cognitive impairments in schizophrenia and schizoaffective disorder: relationship with clinical characteristics. J Nerv Ment Dis. 2012; 200(4):316-22. DOI: 10.1097/NMD.0b013e31824cb359. View

Kay J, Phillips W . Coherent Infomax as a computational goal for neural systems. Bull Math Biol. 2010; 73(2):344-72. DOI: 10.1007/s11538-010-9564-x. View

Carter M, Yizhar O, Chikahisa S, Nguyen H, Adamantidis A, Nishino S . Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci. 2010; 13(12):1526-33. PMC: 3174240. DOI: 10.1038/nn.2682. View

Harris K, Thiele A . Cortical state and attention. Nat Rev Neurosci. 2011; 12(9):509-23. PMC: 3324821. DOI: 10.1038/nrn3084. View

10.

St Clair D, Blackwood D, Muir W, Carothers A, Walker M, Spowart G . Association within a family of a balanced autosomal translocation with major mental illness. Lancet. 1990; 336(8706):13-6. DOI: 10.1016/0140-6736(90)91520-k. View

11.

Scarone S, Manzone M, Gambini O, Kantzas I, Limosani I, DAgostino A . The dream as a model for psychosis: an experimental approach using bizarreness as a cognitive marker. Schizophr Bull. 2007; 34(3):515-22. PMC: 2632423. DOI: 10.1093/schbul/sbm116. View

12.

Ledergerber D, Larkum M . Properties of layer 6 pyramidal neuron apical dendrites. J Neurosci. 2010; 30(39):13031-44. PMC: 6633503. DOI: 10.1523/JNEUROSCI.2254-10.2010. View

13.

Berger T, Larkum M, Luscher H . High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol. 2001; 85(2):855-68. DOI: 10.1152/jn.2001.85.2.855. View

14.

Berger T, Senn W, Luscher H . Hyperpolarization-activated current Ih disconnects somatic and dendritic spike initiation zones in layer V pyramidal neurons. J Neurophysiol. 2003; 90(4):2428-37. DOI: 10.1152/jn.00377.2003. View

15.

Larkum M . A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci. 2013; 36(3):141-51. DOI: 10.1016/j.tins.2012.11.006. View

16.

Fan Y, Fricker D, Brager D, Chen X, Lu H, Chitwood R . Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci. 2005; 8(11):1542-51. DOI: 10.1038/nn1568. View

17.

Larkum M, Zhu J, Sakmann B . A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature. 1999; 398(6725):338-41. DOI: 10.1038/18686. View

18.

Agster K, Mejias-Aponte C, Clark B, Waterhouse B . Evidence for a regional specificity in the density and distribution of noradrenergic varicosities in rat cortex. J Comp Neurol. 2012; 521(10):2195-207. PMC: 4529674. DOI: 10.1002/cne.23270. View

19.

Murayama M, Perez-Garci E, Nevian T, Bock T, Senn W, Larkum M . Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature. 2009; 457(7233):1137-41. DOI: 10.1038/nature07663. View

20.

Pletnikov M, Ayhan Y, Nikolskaia O, Xu Y, Ovanesov M, Huang H . Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol Psychiatry. 2007; 13(2):173-86, 115. DOI: 10.1038/sj.mp.4002079. View