Rapid Effects of Vagus Nerve Stimulation on Sensory Processing Through Activation of Neuromodulatory Systems

Charles Rodenkirch, Jason B Carmel, Qi Wang, Charles Rodenkirch, Jason B Carmel, Qi Wang

Abstract

After sensory information is encoded into neural signals at the periphery, it is processed through multiple brain regions before perception occurs (i.e., sensory processing). Recent work has begun to tease apart how neuromodulatory systems influence sensory processing. Vagus nerve stimulation (VNS) is well-known as an effective and safe method of activating neuromodulatory systems. There is a growing body of studies confirming VNS has immediate effects on sensory processing across multiple sensory modalities. These immediate effects of VNS on sensory processing are distinct from the more well-documented method of inducing lasting neuroplastic changes to the sensory pathways through repeatedly delivering a brief VNS burst paired with a sensory stimulus. Immediate effects occur upon VNS onset, often disappear upon VNS offset, and the modulation is present for all sensory stimuli. Conversely, the neuroplastic effect of pairing sub-second bursts of VNS with a sensory stimulus alters sensory processing only after multiple pairing sessions, this alteration remains after cessation of pairing sessions, and the alteration selectively affects the response properties of neurons encoding the specific paired sensory stimulus. Here, we call attention to the immediate effects VNS has on sensory processing. This review discusses existing studies on this topic, provides an overview of the underlying neuromodulatory systems that likely play a role, and briefly explores the potential translational applications of using VNS to rapidly regulate sensory processing.

Keywords: cholinergic system; dopaminergic system; locus coereleus; neuromodulation; noradrenergic system; sensory processing; serotonergic system; vagus nerve stimulation.

Conflict of interest statement

All authors have financial interest in Sharper Sense, a company developing methods of enhancing sensory processing with VNS.

Copyright © 2022 Rodenkirch, Carmel and Wang.

Figures

FIGURE 1
FIGURE 1
Tonic VNS suppressed burst spiking of thalamocortical neurons and increased the selectivity of their response to the specific stimulus feature they encode, leading to a greater amount of sensory-related information transmitted. (A) VNS did not significantly alter firing rate of ventral posteromedial nucleus (VPm) neurons responding to white gaussian noise whisker (WGN) stimulation. (B) VNS reduced likelihood of VPm burst spikes, multiple successive spikes with a short inter-spike-intervals (∼4 ms or less) commonly occurring after an extended period of quiescence (∼100 ms) due to calcium t-channel current. (C,D) The amplitude of the specific kinetic feature(s) (i.e., whisker deflection) each VPm neuron was selective for was much larger when recovered during VNS, indicating VNS increased selectivity of response. (E) Enhanced feature selectivity of VPm neurons during VNS results in a significant increase in amount of the sensory-related information transmitted per spike. Adopted from Rodenkirch and Wang (2020).
FIGURE 2
FIGURE 2
Vagus nerve stimulation activates multiple global neuromodulatory systems that are known to influence sensory processing. BF, basal forebrain; DRN, dorsal raphe nucleus; LC, locus coeruleus; LDT, laterodorsal tegmental nucleus; NTS, nucleus tractus solitaries; PPT, pedunculopontine tegmental nucleus; VTA, ventral tegmental area.

References

    1. Adcock K. S., Chandler C., Buell E. P., Solorzano B. R., Loerwald K. W., Borland M. S., et al. (2020). Vagus nerve stimulation paired with tones restores auditory processing in a rat model of Rett syndrome. Brain Stimul. 13 1494–1503. 10.1016/j.brs.2020.08.006
    1. Altidor L. K., Bruner M. M., Deslauriers J. F., Garman T. S., Ramirez S., Dirr E. W., et al. (2021). Acute vagus nerve stimulation enhances reversal learning in rats. Neurobiol. Learn. Mem. 184:107498. 10.1016/j.nlm.2021.107498
    1. Arnsten A. F., Dudley A. G. (2005). Methylphenidate improves prefrontal cortical cognitive function through alpha2 adrenoceptor and dopamine D1 receptor actions: relevance to therapeutic effects in attention deficit hyperactivity disorder. Behav. Brain Funct. 1:2. 10.1186/1744-9081-1-2
    1. Aston-Jones G., Waterhouse B. (2016). Locus coeruleus: from global projection system to adaptive regulation of behavior. Brain Res. 1645 75–78. 10.1016/j.brainres.2016.03.001
    1. Avery M. C., Krichmar J. L. (2017). Neuromodulatory systems and their interactions: a review of models, theories, and experiments. Front. Neural Circ. 11:108. 10.3389/fncir.2017.00108
    1. Babkoff H., Fostick L. (2017). Age-related changes in auditory processing and speech perception: cross-sectional and longitudinal analyses. Eur. J. Ageing 14 269–281. 10.1007/s10433-017-0410-y
    1. Ballinger E. C., Ananth M., Talmage D. A., Role L. W. (2016). Basal forebrain cholinergic circuits and signaling in cognition and cognitive decline. Neuron 91 1199–1218. 10.1016/j.neuron.2016.09.006
    1. Bao S., Chan V. T., Merzenich M. M. (2001). Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412 79–83. 10.1038/35083586
    1. Barriga-Rivera A., Bareket L., Goding J., Aregueta-Robles U. A., Suaning G. J. (2017). Visual prosthesis: interfacing stimulating electrodes with retinal neurons to restore vision. Front. Neurosci. 11:620. 10.3389/fnins.2017.00620
    1. Bennett C., Arroyo S., Hestrin S. (2013). Subthreshold mechanisms underlying state-dependent modulation of visual responses. Neuron 80 350–357. 10.1016/j.neuron.2013.08.007
    1. Bentley P., Husain M., Dolan R. J. (2004). Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory. Neuron 41 969–982. 10.1016/S0896-6273(04)00145-X
    1. Berridge C. W., Isaac S. O., España R. A. (2003). Additive wake-promoting actions of medial basal forebrain noradrenergic alpha1- and beta-receptor stimulation. Behav. Neurosci. 117 350–359. 10.1037/0735-7044.117.2.350
    1. Berridge C. W., Waterhouse B. D. (2003). The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42 33–84. 10.1016/s0165-0173(03)00143-7
    1. Brannan J. R. (1992). “Changes in temporal visual processing in normal aging,” in Advances in Psychology, ed. Brannan J. R. (Amsterdam: North-Holland; ), 119–134. 10.1016/S0166-4115(08)61351-5
    1. Carpenter L. L., Moreno F. A., Kling M. A., Anderson G. M., Regenold W. T., Labiner D. M., et al. (2004). Effect of vagus nerve stimulation on cerebrospinal fluid monoamine metabolites, norepinephrine, and gamma-aminobutyric acid concentrations in depressed patients. Biol. Psychiatry 56 418–426. 10.1016/j.biopsych.2004.06.025
    1. Carrasco M., Ling S., Read S. (2004). Attention alters appearance. Nat. Neurosci. 7 308–313. 10.1038/nn1194
    1. Chandler D. J., Jensen P., McCall J. G., Pickering A. E., Schwarz L. A., Totah N. K. (2019). Redefining noradrenergic neuromodulation of behavior: impacts of a modular locus coeruleus architecture. J. Neurosci. 39:8239. 10.1523/JNEUROSCI.1164-19.2019
    1. Chechik G., Anderson M. J., Bar-Yosef O., Young E. D., Tishby N., Nelken I. (2006). Reduction of information redundancy in the ascending auditory pathway. Neuron 51 359–368. 10.1016/j.neuron.2006.06.030
    1. Collins L., Boddington L., Steffan P. J., McCormick D. (2021). Vagus nerve stimulation induces widespread cortical and behavioral activation. Curr. Biol. 31 2088.e3–2098.e3. 10.1016/j.cub.2021.02.049
    1. Cunningham J. T., Mifflin S. W., Gould G. G., Frazer A. (2008). Induction of c-Fos and DeltaFosB immunoreactivity in rat brain by Vagal nerve stimulation. Neuropsychopharmacology 33 1884–1895. 10.1038/sj.npp.1301570
    1. Dacks A. M., Green D. S., Root C. M., Nighorn A. J., Wang J. W. (2009). Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J. Neurogenet. 23 366–377. 10.3109/01677060903085722
    1. Dahan L., Astier B., Vautrelle N., Urbain N., Kocsis B., Chouvet G. (2007). Prominent burst firing of dopaminergic neurons in the ventral tegmental area during paradoxical sleep. Neuropsychopharmacology 32 1232–1241. 10.1038/sj.npp.1301251
    1. Darrow M. J., Mian T. M., Torres M., Haider Z., Danaphongse T., Rennaker R. L., Jr., et al. (2020). Restoration of somatosensory function by pairing vagus nerve stimulation with tactile rehabilitation. Ann. Neurol. 87 194–205. 10.1002/ana.25664
    1. De Crescenzo F., Ziganshina L. E., Yudina E. V., Kaplan Y. C., Ciabattini M., Wei Y., et al. (2018). Noradrenaline reuptake inhibitors (NRIs) for attention deficit hyperactivity disorder (ADHD) in adults. Cochrane Database Syst. Rev. 2018:CD013044. 10.1002/14651858.CD013044
    1. De Taeye L., Vonck K., van Bochove M., Boon P., Van Roost D., Mollet L., et al. (2014). The P3 event-related potential is a biomarker for the efficacy of vagus nerve stimulation in patients with epilepsy. Neurotherapeutics 11 612–622. 10.1007/s13311-014-0272-3
    1. Dedeurwaerdere S., Cornelissen B., Van Laere K., Vonck K., Achten E., Slegers G., et al. (2005). Small animal positron emission tomography during vagus nerve stimulation in rats: a pilot study. Epilepsy Res. 67 133–141. 10.1016/j.eplepsyres.2005.09.008
    1. Detari L., Juhasz G., Kukorelli T. (1983). Effect of stimulation of vagal and radial nerves on neuronal activity in the basal forebrain area of anaesthetized cats. Acta Physiol. Hung 61 147–154.
    1. Devilbiss D. M., Waterhouse B. D. (2004). The effects of tonic locus ceruleus output on sensory-evoked responses of ventral posterior medial thalamic and barrel field cortical neurons in the awake rat. J. Neurosci. 24 10773–10785. 10.1523/JNEUROSCI.1573-04.2004
    1. Devilbiss D. M., Waterhouse B. D. (2011). Phasic and tonic patterns of locus coeruleus output differentially modulate sensory network function in the awake rat. J. Neurophysiol. 105 69–87. 10.1152/jn.00445.2010
    1. Donoghue J. P., Carroll K. L. (1987). Cholinergic modulation of sensory responses in rat primary somatic sensory cortex. Brain Res. 408 367–371. 10.1016/0006-8993(87)90407-0
    1. Dorr A. E., Debonnel G. (2006). Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission. J. Pharmacol. Exp. Ther. 318 890–898. 10.1124/jpet.106.104166
    1. Doucette W., Milder J., Restrepo D. (2007). Adrenergic modulation of olfactory bulb circuitry affects odor discrimination. Learn. Mem. 14 539–547. 10.1101/lm.606407
    1. Ego-Stengel V., Bringuier V., Shulz D. E. (2002). Noradrenergic modulation of functional selectivity in the cat visual cortex: an in vivo extracellular and intracellular study. Neuroscience 111 275–289. 10.1016/s0306-4522(02)00011-8
    1. Engel-Yeger B., Hus S., Rosenblum S. (2012). Age effects on sensory-processing abilities and their impact on handwriting. Can. J. Occup. Ther. Rev. Can. D’ergother. 79 264–274. 10.2182/CJOT.2012.79.5.2
    1. Engel-Yeger B., Rosenblum S. (2017). The relationship between sensory-processing patterns and occupational engagement among older persons. Can. J. Occup. Ther. Rev. Can. D’ergother. 84 10–21. 10.1177/0008417417690415
    1. Engineer C. (2019). Vagus nerve stimulation as a strategy to augment auditory rehabilitation. Brain Stimul. 12:420. 10.1016/j.brs.2018.12.360
    1. Engineer C. T., Engineer N. D., Riley J. R., Seale J. D., Kilgard M. P. (2015). Pairing speech sounds with vagus nerve stimulation drives stimulus-specific cortical plasticity. Brain Stimul. 8 637–644. 10.1016/j.brs.2015.01.408
    1. Engineer N. D., Moller A. R., Kilgard M. P. (2013). Directing neural plasticity to understand and treat tinnitus. Hear Res. 295 58–66. 10.1016/j.heares.2012.10.001
    1. Engineer N. D., Riley J. R., Seale J. D., Vrana W. A., Shetake J. A., Sudanagunta S. P., et al. (2011). Reversing pathological neural activity using targeted plasticity. Nature 470 101–104. 10.1038/nature09656
    1. Ennis M., Aston-Jones G. (1988). Activation of locus coeruleus from nucleus paragigantocellularis: a new excitatory amino acid pathway in brain. J. Neurosci. 8 3644–3657. 10.1523/JNEUROSCI.08-10-03644.1988
    1. Ferguson M. A., Kitterick P. T., Chong L. Y., Edmondson-Jones M., Barker F., Hoare D. J. (2017). Hearing aids for mild to moderate hearing loss in adults. Cochr. Database Syst. Rev. 9:CD012023. 10.1002/14651858.CD012023.pub2
    1. Fernandes A. B., Alves da Silva J., Almeida J., Cui G., Gerfen C. R., Costa R. M., et al. (2020). Postingestive modulation of food seeking depends on vagus-mediated dopamine neuron activity. Neuron 106 778.e6–788.e6. 10.1016/j.neuron.2020.03.009
    1. Follesa P., Biggio F., Gorini G., Caria S., Talani G., Dazzi L., et al. (2007). Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Res. 1179 28–34. 10.1016/j.brainres.2007.08.045
    1. Frangos E., Komisaruk B. R. (2017). Access to vagal projections via cutaneous electrical stimulation of the neck: fMRI evidence in healthy humans. Brain Stimul. 10 19–27. 10.1016/j.brs.2016.10.008
    1. Fullgrabe C., Moore B. C., Stone M. A. (2014). Age-group differences in speech identification despite matched audiometrically normal hearing: contributions from auditory temporal processing and cognition. Front. Aging Neurosci. 6:347. 10.3389/fnagi.2014.00347
    1. Funke K., Eysel U. T. (1993). Modulatory effects of acetylcholine, serotonin and noradrenaline on the activity of cat perigeniculate neurons. Exp. Brain Res. 95 409–420. 10.1007/BF00227133
    1. Furey M. L., Pietrini P., Haxby J. V., Drevets W. C. (2008). Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychopharmacology 33 913–923. 10.1038/sj.npp.1301461
    1. Furmaga H., Shah A., Frazer A. (2011). Serotonergic and noradrenergic pathways are required for the anxiolytic-like and antidepressant-like behavioral effects of repeated vagal nerve stimulation in rats. Biol. Psychiatry 70 937–945. 10.1016/j.biopsych.2011.07.020
    1. Garcia-Diaz D. E., Aguilar-Baturoni H. U., Guevara-Aguilar R., Wayner M. J. (1984). Vagus nerve stimulation modifies the electrical activity of the olfactory bulb. Brain Res. Bull. 12 529–537. 10.1016/0361-9230(84)90168-0
    1. Goard M., Dan Y. (2009). Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12 1444–1449. 10.1038/nn.2402
    1. Govindaiah G., Wang Y., Cox C. L. (2010). Dopamine enhances the excitability of somatosensory thalamocortical neurons. Neuroscience 170 981–991. 10.1016/j.neuroscience.2010.08.043
    1. Gratton C., Yousef S., Aarts E., Wallace D. L., D’Esposito M., Silver M. A. (2017). Cholinergic, but not dopaminergic or noradrenergic, enhancement sharpens visual spatial perception in humans. J. Neurosci. 37 4405–4415. 10.1523/JNEUROSCI.2405-16.2017
    1. Grimonprez A., Raedt R., Portelli J., Dauwe I., Larsen L. E., Bouckaert C., et al. (2015). The antidepressant-like effect of vagus nerve stimulation is mediated through the locus coeruleus. J. Psychiatr. Res. 68 1–7. 10.1016/j.jpsychires.2015.05.002
    1. Groves D. A., Bowman E. M., Brown V. J. (2005). Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat. Neurosci. Lett. 379 174–179. 10.1016/j.neulet.2004.12.055
    1. Hassert D. L., Miyashita T., Williams C. L. (2004). The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav. Neurosci. 118 79–88. 10.1037/0735-7044.118.1.79
    1. Hays S. A. (2016). Enhancing rehabilitative therapies with vagus nerve stimulation. Neurotherapeutics 13 382–394. 10.1007/s13311-015-0417-z
    1. Herrero J. L., Roberts M. J., Delicato L. S., Gieselmann M. A., Dayan P., Thiele A. (2008). Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454 1110–1114. 10.1038/nature07141
    1. Hewitt D. (2017). Age-related hearing loss and cognitive decline: you haven’t heard the half of it. Front. Aging Neurosci. 9:112. 10.3389/fnagi.2017.00112
    1. Higuchi A., Kumar S. S., Benelli G., Alarfaj A. A., Munusamy M. A., Umezawa A., et al. (2017). Stem cell therapies for reversing vision loss. Trends Biotechnol. 35 1102–1117. 10.1016/j.tibtech.2017.06.016
    1. Hirata A., Aguilar J., Castro-Alamancos M. A. (2006). Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus. J. Neurosci. 26 4426–4436. 10.1523/JNEUROSCI.5298-05.2006
    1. Hosp J. A., Coenen V. A., Rijntjes M., Egger K., Urbach H., Weiller C., et al. (2019). Ventral tegmental area connections to motor and sensory cortical fields in humans. Brain Struct. Funct. 224 2839–2855. 10.1007/s00429-019-01939-0
    1. Huerta-Ocampo I., Hacioglu-Bay H., Dautan D., Mena-Segovia J. (2020). Distribution of midbrain cholinergic axons in the thalamus. eNeuro 7:ENEURO.0454-19.2019. 10.1523/ENEURO.0454-19.2019
    1. Hulsey D. R., Hays S. A., Khodaparast N., Ruiz A., Das P., Rennaker R. L., II, et al. (2016). Reorganization of motor cortex by vagus nerve stimulation requires cholinergic innervation. Brain Stimul. 9 174–181. 10.1016/j.brs.2015.12.007
    1. Hulsey D. R., Riley J. R., Loerwald K. W., Rennaker R. L., II, Kilgard M. P., Hays S. A. (2017). Parametric characterization of neural activity in the locus coeruleus in response to vagus nerve stimulation. Exp. Neurol. 289 21–30. 10.1016/j.expneurol.2016.12.005
    1. Hulsey D. R., Shedd C. M., Sarker S. F., Kilgard M. P., Hays S. A. (2019). Norepinephrine and serotonin are required for vagus nerve stimulation directed cortical plasticity. Exp. Neurol. 320:112975. 10.1016/j.expneurol.2019.112975
    1. Humes L. E. (2015). Age-related changes in cognitive and sensory processing: focus on middle-aged adults. Am. J. Audiol. 24 94–97. 10.1044/2015_AJA-14-0063
    1. Humes L. E., Busey T. A., Craig J., Kewley-Port D. (2013). Are age-related changes in cognitive function driven by age-related changes in sensory processing? Atten. Percept. Psychophys. 75 508–524. 10.3758/s13414-012-0406-9
    1. Hurley L. M., Hall I. C. (2011). Context-dependent modulation of auditory processing by serotonin. Hear. Res. 279 74–84. 10.1016/j.heares.2010.12.015
    1. Hurley L. M., Pollak G. D. (1999). Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J. Neurosci. 19 8071–8082. 10.1523/JNEUROSCI.19-18-08071.1999
    1. Hyland B. I., Reynolds J. N. J., Hay J., Perk C. G., Miller R. (2002). Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114 475–492. 10.1016/S0306-4522(02)00267-1
    1. Hyvarinen P., Yrttiaho S., Lehtimaki J., Ilmoniemi R. J., Makitie A., Ylikoski J., et al. (2015). Transcutaneous vagus nerve stimulation modulates tinnitus-related beta- and gamma-band activity. Ear Hear. 36 e76–e85. 10.1097/AUD.0000000000000123
    1. Jaber L., Zhao F. L., Kolli T., Herness S. (2014). A physiologic role for serotonergic transmission in adult rat taste buds. PLoS One 9:e112152. 10.1371/journal.pone.0112152
    1. Jacobs B. L., Fornal C. A. (1999). Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21 9S–15S. 10.1016/S0893-133X(99)00012-3
    1. Jiang Y., Li L., Liu B., Zhang Y., Chen Q., Li C. (2014). Vagus nerve stimulation attenuates cerebral ischemia and reperfusion injury via endogenous cholinergic pathway in rat. PLoS One 9:e102342. 10.1371/journal.pone.0102342
    1. Jimenez-Martin J., Potapov D., Potapov K., Knöpfel T., Empson R. M. (2021). Cholinergic modulation of sensory processing in awake mouse cortex. Sci. Rep. 11:17525. 10.1038/s41598-021-96696-8
    1. Kähkönen S., Ahveninen J., Pennanen S., Liesivuori J., Ilmoniemi R. J., Jääskeläinen I. P. (2002). Serotonin modulates early cortical auditory processing in healthy subjects. Evidence from MEG with acute tryptophan depletion. Neuropsychopharmacology 27 862–868. 10.1016/S0893-133X(02)00357-3
    1. Kapoor V., Provost A. C., Agarwal P., Murthy V. N. (2016). Activation of raphe nuclei triggers rapid and distinct effects on parallel olfactory bulb output channels. Nat. Neurosci. 19 271–282. 10.1038/nn.4219
    1. Kayama Y., Shimada S., Hishikawa Y., Ogawa T. (1989). Effects of stimulating the dorsal raphe nucleus of the rat on neuronal activity in the dorsal lateral geniculate nucleus. Brain Res. 489 1–11. 10.1016/0006-8993(89)90002-4
    1. Kelly S. T., Kremkow J., Jin J., Wang Y., Wang Q., Alonso J.-M., et al. (2014). The role of thalamic population synchrony in the emergence of cortical feature selectivity. PLoS Comput. Biol. 10:e1003418. 10.1371/journal.pcbi.1003418
    1. Kilgard M. P., Merzenich M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science 279 1714–1718. 10.1126/science.279.5357.1714
    1. Kilgard M. P., Rennaker R. L., Alexander J., Dawson J. (2018). Vagus nerve stimulation paired with tactile training improved sensory function in a chronic stroke patient. NeuroRehabilitation 42 159–165. 10.3233/NRE-172273
    1. Kim J. H., Jung A. H., Jeong D., Choi I., Kim K., Shin S., et al. (2016). Selectivity of neuromodulatory projections from the basal forebrain and locus ceruleus to primary sensory cortices. J. Neurosci. 36 5314–5327. 10.1523/JNEUROSCI.4333-15.2016
    1. Kim M. A., Lee H. S., Lee B. Y., Waterhouse B. D. (2004). Reciprocal connections between subdivisions of the dorsal raphe and the nuclear core of the locus coeruleus in the rat. Brain Res. 1026 56–67. 10.1016/j.brainres.2004.08.022
    1. Kirifides M. L., Simpson K. L., Lin R. C., Waterhouse B. D. (2001). Topographic organization and neurochemical identity of dorsal raphe neurons that project to the trigeminal somatosensory pathway in the rat. J. Comp. Neurol. 435 325–340. 10.1002/cne.1033
    1. Kiyatkin E. A., Rebec G. V. (1998). Heterogeneity of ventral tegmental area neurons: single-unit recording and iontophoresis in awake, unrestrained rats. Neuroscience 85 1285–1309. 10.1016/s0306-4522(98)00054-2
    1. Kolmac C., Mitrofanis J. (1999). Organization of the basal forebrain projection to the thalamus in rats. Neurosci. Lett. 272 151–154. 10.1016/s0304-3940(99)00614-x
    1. Krahl S. E., Clark K. B., Smith D. C., Browning R. A. (1998). Locus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation. Epilepsia 39 709–714. 10.1111/j.1528-1157.1998.tb01155.x
    1. Kreuzer P. M., Landgrebe M., Resch M., Husser O., Schecklmann M., Geisreiter F., et al. (2014). Feasibility, safety and efficacy of transcutaneous vagus nerve stimulation in chronic tinnitus: an open pilot study. Brain Stimul. 7 740–747. 10.1016/j.brs.2014.05.003
    1. Lai J., David S. V. (2021). Short-term effects of vagus nerve stimulation on learning and evoked activity in auditory cortex. eNeuro 8:ENEURO.0522-20.2021. 10.1523/ENEURO.0522-20.2021
    1. Laszlovszky T., Schlingloff D., Hegedüs P., Freund T. F., Gulyás A., Kepecs A., et al. (2020). Distinct synchronization, cortical coupling and behavioral function of two basal forebrain cholinergic neuron types. Nat. Neurosci. 23 992–1003. 10.1038/s41593-020-0648-0
    1. Lesica N. A. (2018). Why do hearing aids fail to restore normal auditory perception? Trends Neurosci. 41 174–185. 10.1016/j.tins.2018.01.008
    1. Li Y., Zhong W., Wang D., Feng Q., Liu Z., Zhou J., et al. (2016). Serotonin neurons in the dorsal raphe nucleus encode reward signals. Nat. Commun. 7:10503. 10.1038/ncomms10503
    1. Linster C., Cleland T. A. (2002). Cholinergic modulation of sensory representations in the olfactory bulb. Neural Netw. 15 709–717. 10.1016/S0893-6080(02)00061-8
    1. Liu Y., Narasimhan S., Schriver B. J., Wang Q. (2021). Perceptual behavior depends differently on pupil-linked arousal and heartbeat dynamics-linked arousal in rats performing tactile discrimination tasks. Front. Syst. Neurosci. 14:614248. 10.3389/fnsys.2020.614248
    1. Liu Y., Rodenkirch C., Moskowitz N., Schriver B., Wang Q. (2017). Dynamic lateralization of pupil dilation evoked by locus coeruleus activation results from sympathetic, not parasympathetic, contributions. Cell Rep. 20 3099–3112. 10.1016/j.celrep.2017.08.094
    1. Llanos F., McHaney J. R., Schuerman W. L., Yi H. G., Leonard M. K., Chandrasekaran B. (2020). Non-invasive peripheral nerve stimulation selectively enhances speech category learning in adults. NPJ Sci. Learn. 5:12. 10.1038/s41539-020-0070-0
    1. Lodge D. J., Grace A. A. (2006). The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 103 5167–5172. 10.1073/pnas.0510715103
    1. Lottem E., Lörincz M. L., Mainen Z. F. (2016). Optogenetic activation of dorsal raphe serotonin neurons rapidly inhibits spontaneous but not odor-evoked activity in olfactory cortex. J. Neurosci. 36 7–18. 10.1523/JNEUROSCI.3008-15.2016
    1. Lu X. X., Hong Z. Q., Tan Z., Sui M. H., Zhuang Z. Q., Liu H. H., et al. (2017). Nicotinic acetylcholine receptor Alpha7 subunit mediates vagus nerve stimulation-induced neuroprotection in acute permanent cerebral ischemia by a7nAchR/JAK2 pathway. Med. Sci. Monit. 23 6072–6081. 10.12659/msm.907628
    1. Manta S., Dong J., Debonnel G., Blier P. (2009a). Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation. J. Psychiatry Neurosci. 34 272–280.
    1. Manta S., Dong J., Debonnel G., Blier P. (2009b). Optimization of vagus nerve stimulation parameters using the firing activity of serotonin neurons in the rat dorsal raphe. Eur. Neuropsychopharmacol. 19 250–255. 10.1016/j.euroneuro.2008.12.001
    1. Manta S., El Mansari M., Blier P. (2012). Novel attempts to optimize vagus nerve stimulation parameters on serotonin neuronal firing activity in the rat brain. Brain Stimul. 5 422–429. 10.1016/j.brs.2011.04.005
    1. Manta S., El Mansari M., Debonnel G., Blier P. (2013). Electrophysiological and neurochemical effects of long-term vagus nerve stimulation on the rat monoaminergic systems. Int. J. Neuropsychopharmacol. 16 459–470. 10.1017/S1461145712000387
    1. Manunta Y., Edeline J. M. (1997). Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. Eur. J. Neurosci. 9 833–847. 10.1111/j.1460-9568.1997.tb01433.x
    1. Marks G. A., Speciale S. G., Cobbey K., Roffwarg H. P. (1987). Serotonergic inhibition of the dorsal lateral geniculate nucleus. Brain Res. 418 76–84. 10.1016/0006-8993(87)90964-4
    1. Martin K. A., Papadoyannis E. S., Schiavo J. K., Fadaei S. S., Temiz N. Z., McGinley M. J., et al. (2022). Vagus nerve stimulation recruits the central cholinergic system to enhance perceptual learning. bioRxiv [Preprint]. 10.1101/2022.01.28.478197v1
    1. Martinez-Vargas D., Valdes-Cruz A., Magdaleno-Madrigal V. M., Almazan-Alvarado S., Fernandez-Mas R. (2009). Effects of electrical stimulation of the vagus nerve on the development of visual habituation in the cat. Behav. Brain Res. 205 45–49. 10.1016/j.bbr.2009.06.029
    1. Martins A. R., Froemke R. C. (2015). Coordinated forms of noradrenergic plasticity in the locus coeruleus and primary auditory cortex. Nat. Neurosci. 18 1483–1492. 10.1038/nn.4090
    1. McBurney-Lin J., Lu J., Zuo Y., Yang H. (2019). Locus coeruleus-norepinephrine modulation of sensory processing and perception: a focused review. Neurosci. Biobehav. Rev. 105 190–199. 10.1016/j.neubiorev.2019.06.009
    1. McCormick D. A., Prince D. A. (1986). Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319 402–405. 10.1038/319402a0
    1. McCormick D. A., Prince D. A. (1987). Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J. Physiol. 392 147–165. 10.1113/jphysiol.1987.sp016774
    1. McCormick D. A., Prince D. A. (1988). Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. J. Neurophysiol. 59 978–996. 10.1152/jn.1988.59.3.978
    1. McCormick D. A., Wang Z. (1991). Serotonin and noradrenaline excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. J. Physiol. 442 235–255. 10.1113/jphysiol.1991.sp018791
    1. McGinley M. J., Vinck M., Reimer J., Batista-Brito R., Zagha E., Cadwell Cathryn R., et al. (2015). Waking state: rapid variations modulate neural and behavioral responses. Neuron 87 1143–1161. 10.1016/j.neuron.2015.09.012
    1. McIntire L. K., McKinley R. A., Goodyear C., McIntire J. P., Brown R. D. (2021). Cervical transcutaneous vagal nerve stimulation (ctVNS) improves human cognitive performance under sleep deprivation stress. Commun. Biol. 4:634. 10.1038/s42003-021-02145-7
    1. Mejías-Aponte C. A., Drouin C., Aston-Jones G. (2009). Adrenergic and noradrenergic innervation of the midbrain ventral tegmental area and retrorubral field: prominent inputs from medullary homeostatic centers. J. Neurosci. 29 3613–3626. 10.1523/JNEUROSCI.4632-08.2009
    1. Mercuri N. B., Calabresi P., Bernardi G. (1992). The electrophysiological actions of dopamine and dopaminergic drugs on neurons of the substantia nigra pars compacta and ventral tegmental area. Life Sci. 51 711–718. 10.1016/0024-3205(92)90479-9
    1. Metherate R., Ashe J. H. (1991). Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 559 163–167. 10.1016/0006-8993(91)90301-b
    1. Metherate R., Weinberger N. M. (1989). Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex. Brain Res. 480 372–377. 10.1016/0006-8993(89)90210-2
    1. Meyers E. C., Kasliwal N., Solorzano B. R., Lai E., Bendale G., Berry A., et al. (2019). Enhancing plasticity in central networks improves motor and sensory recovery after nerve damage. Nat. Commun. 10:5782. 10.1038/s41467-019-13695-0
    1. Millard D. C., Wang Q., Gollnick C. A., Stanley G. B. (2013). System identification of the nonlinear dynamics in the thalamocortical circuit in response to patterned thalamic microstimulation in vivo. J. Neural Eng. 10:066011. 10.1088/1741-2560/10/6/066011
    1. Mlinar B., Montalbano A., Piszczek L., Gross C., Corradetti R. (2016). Firing properties of genetically identified dorsal raphe serotonergic neurons in brain slices. Front. Cell. Neurosci. 10:195. 10.3389/fncel.2016.00195
    1. Monckton J. E., McCormick D. A. (2002). Neuromodulatory role of serotonin in the ferret thalamus. J. Neurophysiol. 87 2124–2136. 10.1152/jn.00650.2001
    1. Mooney D. M., Zhang L., Basile C., Senatorov V. V., Ngsee J., Omar A., et al. (2004). Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. Proc. Natl. Acad. Sci. U.S.A. 101 320–324. 10.1073/pnas.0304445101
    1. Morrison J. H., Foote S. L. (1986). Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. J. Comp. Neurol. 243 117–138. 10.1002/cne.902430110
    1. Morrison R. A., Hulsey D. R., Adcock K. S., Rennaker R. L., II, Kilgard M. P., Hays S. A. (2019). Vagus nerve stimulation intensity influences motor cortex plasticity. Brain Stimul. 12 256–262. 10.1016/j.brs.2018.10.017
    1. Moshirfar M., Jehangir N., Fenzl C. R., McCaughey M. (2017). LASIK enhancement: clinical and surgical management. J. Refract. Surg. 33 116–127. 10.3928/1081597X-20161202-01
    1. Mridha Z., de Gee J. W., Shi Y., Alkashgari R., Williams J., Suminski A., et al. (2021). Graded recruitment of pupil-linked neuromodulation by parametric stimulation of the vagus nerve. Nat. Commun. 12:1539. 10.1038/s41467-021-21730-2
    1. Murphy P. C., Sillito A. M. (1991). Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience 40 13–20. 10.1016/0306-4522(91)90170-S
    1. Mwamburi M., Liebler E. J., Tenaglia A. T. (2017). Review of non-invasive vagus nerve stimulation (gammaCore): efficacy, safety, potential impact on comorbidities, and economic burden for episodic and chronic cluster headache. Am. J. Manag. Care 23 S317–S325.
    1. Navarra R. L., Clark B. D., Gargiulo A. T., Waterhouse B. D. (2017). Methylphenidate enhances early-stage sensory processing and rodent performance of a visual signal detection task. Neuropsychopharmacology 42 1326–1337. 10.1038/npp.2016.267
    1. Neuhaus A. H., Luborzewski A., Rentzsch J., Brakemeier E. L., Opgen-Rhein C., Gallinat J., et al. (2007). P300 is enhanced in responders to vagus nerve stimulation for treatment of major depressive disorder. J. Affect. Disord. 100 123–128. 10.1016/j.jad.2006.10.005
    1. Nichols J. A., Nichols A. R., Smirnakis S. M., Engineer N. D., Kilgard M. P., Atzori M. (2011). Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors. Neuroscience 189 207–214. 10.1016/j.neuroscience.2011.05.024
    1. Nicolelis M. A. L., Fanselow E. E. (2002). Thalamocortical optimization of tactile processing according to behavioral state. Nat. Neurosci. 5 517–523. 10.1038/nn0602-517
    1. Niell C. M., Stryker M. P. (2010). Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65 472–479. 10.1016/j.neuron.2010.01.033
    1. Nuñez A. (1996). Unit activity of rat basal forebrain neurons: relationship to cortical activity. Neuroscience 72 757–766. 10.1016/0306-4522(95)00582-X
    1. Ollerenshaw D. R., Bari B. A., Millard D. C., Orr L. E., Wang Q., Stanley G. B. (2012). Detection of tactile inputs in the rat vibrissa pathway. J. Neurophysiol. 108 479–490. 10.1152/jn.00004.2012
    1. Ollerenshaw D. R., Zheng H. J. V., Millard Daniel C., Wang Q., Stanley Garrett B. (2014). The adaptive trade-off between detection and discrimination in cortical representations and behavior. Neuron 81 1152–1164. 10.1016/j.neuron.2014.01.025
    1. Panza F., Solfrizzi V., Logroscino G. (2015). Age-related hearing impairment-a risk factor and frailty marker for dementia and AD. Nat. Rev. Neurol. 11 166–175. 10.1038/nrneurol.2015.12
    1. Parikh V., Sarter M. (2008). Cholinergic mediation of attention. Ann. N.Y. Acad. Sci. 1129 225–235. 10.1196/annals.1417.021
    1. Peng L., Mu K., Liu A., Zhou L., Gao Y., Shenoy I. T., et al. (2018). Transauricular vagus nerve stimulation at auricular acupoints Kindey (CO10), Yidan (CO11), Liver (CO12) and Shenmen (TF4) can induce auditory and limbic cortices activation measured by fMRI. Hear. Res. 359 1–12. 10.1016/j.heares.2017.12.003
    1. Perez S. M., Carreno F. R., Frazer A., Lodge D. J. (2014). Vagal nerve stimulation reverses aberrant dopamine system function in the methylazoxymethanol acetate rodent model of schizophrenia. J. Neurosci. 34 9261–9267. 10.1523/JNEUROSCI.0588-14.2014
    1. Phillips I., Calloway R. C., Karuzis V. P., Pandza N. B., O’Rourke P., Kuchinsky S. E. (2021). Transcutaneous auricular vagus nerve stimulation strengthens semantic representations of foreign language tone words during initial stages of learning. J. Cogn. Neurosci. 34 127–152. 10.1162/jocn_a_01783
    1. Pinto L., Goard M. J., Estandian D., Xu M., Kwan A. C., Lee S.-H., et al. (2013). Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16 1857–1863. 10.1038/nn.3552
    1. Poulin J. F., Caronia G., Hofer C., Cui Q., Helm B., Ramakrishnan C., et al. (2018). Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches. Nat. Neurosci. 21 1260–1271. 10.1038/s41593-018-0203-4
    1. Raedt R., Clinckers R., Mollet L., Vonck K., El Tahry R., Wyckhuys T., et al. (2011). Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model. J. Neurochem. 117 461–469. 10.1111/j.1471-4159.2011.07214.x
    1. Rajkowski J., Kubiak P., Aston-Jones G. (1994). Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res. Bull. 35 607–616. 10.1016/0361-9230(94)90175-9
    1. Ramcharan E. J., Gnadt J. W., Sherman S. M. (2000). Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis. Neurosci. 17 55–62. 10.1017/s0952523800171056
    1. Ranade S. P., Mainen Z. F. (2009). Transient firing of dorsal raphe neurons encodes diverse and specific sensory, motor, and reward events. J. Neurophysiol. 102 3026–3037. 10.1152/jn.00507.2009
    1. Rasmussen K., Heym J., Jacobs B. L. (1984). Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp. Neurol. 83 302–317. 10.1016/S0014-4886(84)90100-6
    1. Reid C. R., Alonso J.-M. (1995). Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378 281–284. 10.1038/378281a0
    1. Reimer J., Froudarakis E., Cadwell Cathryn R., Yatsenko D., Denfield George H., Tolias Andreas S. (2014). Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84 355–362. 10.1016/j.neuron.2014.09.033
    1. Reimer J., McGinley M. J., Liu Y., Rodenkirch C., Wang Q., McCormick D. A., et al. (2016). Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nat. Commun. 7:13289. 10.1038/ncomms13289
    1. Ren J., Friedmann D., Xiong J., Liu C. D., Ferguson B. R., Weerakkody T., et al. (2018). Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems. Cell 175 472.e20–487.e20. 10.1016/j.cell.2018.07.043
    1. Reuter U., McClure C., Liebler E., Pozo-Rosich P. (2019). Non-invasive neuromodulation for migraine and cluster headache: a systematic review of clinical trials. J. Neurol. Neurosurg. Psychiatry 90 796–804. 10.1136/jnnp-2018-320113
    1. Reyes B. A., Van Bockstaele E. J. (2006). Divergent projections of catecholaminergic neurons in the nucleus of the solitary tract to limbic forebrain and medullary autonomic brain regions. Brain Res. 1117 69–79. 10.1016/j.brainres.2006.08.051
    1. Rikhye R. V., Wimmer R. D., Halassa M. M. (2018). Toward an integrative theory of thalamic function. Annu. Rev. Neurosci. 41 163–183. 10.1146/annurev-neuro-080317-062144
    1. Rodenkirch C., Liu Y., Schriver B. J., Wang Q. (2019). Locus coeruleus activation enhances thalamic feature selectivity via norepinephrine regulation of intrathalamic circuit dynamics. Nat. Neurosci. 22 120–133. 10.1038/s41593-018-0283-1
    1. Rodenkirch C., Wang Q. (2020). Rapid and transient enhancement of thalamic information transmission induced by vagus nerve stimulation. J. Neural Eng. 17:e026027. 10.1088/1741-2552/ab6b84
    1. Rodieck R. W. (1979). Visual pathways. Annu. Rev. Neurosci. 2 193–225. 10.1146/annurev.ne.02.030179.001205
    1. Roosevelt R. W., Smith D. C., Clough R. W., Jensen R. A., Browning R. A. (2006). Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res. 1119 124–132. 10.1016/j.brainres.2006.08.048
    1. Rothermel M., Carey R. M., Puche A., Shipley M. T., Wachowiak M. (2014). Cholinergic inputs from Basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J. Neurosci. 34 4654–4664. 10.1523/JNEUROSCI.5026-13.2014
    1. Rufener K. S., Geyer U., Janitzky K., Heinze H. J., Zaehle T. (2018). Modulating auditory selective attention by non-invasive brain stimulation: differential effects of transcutaneous vagal nerve stimulation and transcranial random noise stimulation. Eur. J. Neurosci. 48 2301–2309. 10.1111/ejn.14128
    1. Ruffoli R., Giorgi F. S., Pizzanelli C., Murri L., Paparelli A., Fornai F. (2011). The chemical neuroanatomy of vagus nerve stimulation. J. Chem. Neuroanat. 42 288–296. 10.1016/j.jchemneu.2010.12.002
    1. Saalmann Y. B., Kastner S. (2011). Cognitive and perceptual functions of the visual thalamus. Neuron 71 209–223. 10.1016/j.neuron.2011.06.027
    1. Sara S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 10 211–223. 10.1038/nrn2573
    1. Sardone R., Battista P., Panza F., Lozupone M., Griseta C., Castellana F., et al. (2019). The age-related central auditory processing disorder: silent impairment of the cognitive ear. Front. Neurosci. 13:619. 10.3389/fnins.2019.00619
    1. Sato H., Fox K., Daw N. W. (1989). Effect of electrical stimulation of locus coeruleus on the activity of neurons in the cat visual cortex. J. Neurophysiol. 62 946–958. 10.1152/jn.1989.62.4.946
    1. Schneider J., Patterson M., Jimenez X. F. (2019). Beyond depression: other uses for tricyclic antidepressants. Cleveland Clin. J. Med. 86 807–814. 10.3949/ccjm.86a.19005
    1. Schofield B. R., Motts S. D., Mellott J. G. (2011). Cholinergic cells of the pontomesencephalic tegmentum: connections with auditory structures from cochlear nucleus to cortex. Hear. Res. 279 85–95. 10.1016/j.heares.2010.12.019
    1. Schriver B., Bagdasarov S., Wang Q. (2018). Pupil-linked arousal modulates behavior in rats performing a whisker deflection direction discrimination task. J. Neurophysiol. 120 1655–1670. 10.1152/jn.00290.2018
    1. Schriver B. J., Perkins S. M., Sajda P., Wang Q. (2020). Interplay between components of pupil-linked phasic arousal and its role in driving behavioral choice in Go/No-Go perceptual decision-making. Psychophysiology 57:e13565. 10.1111/psyp.13565
    1. Seillier L., Lorenz C., Kawaguchi K., Ott T., Nieder A., Pourriahi P., et al. (2017). Serotonin decreases the gain of visual responses in awake macaque V1. J. Neurosci. 37 11390–11405. 10.1523/JNEUROSCI.1339-17.2017
    1. Shen H., Fuchino Y., Miyamoto D., Nomura H., Matsuki N. (2012). Vagus nerve stimulation enhances perforant path-CA3 synaptic transmission via the activation of beta-adrenergic receptors and the locus coeruleus. Int. J. Neuropsychopharmacol. 15 523–530. 10.1017/S1461145711000708
    1. Sherman S. M. (2001a). Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24 122–126.
    1. Sherman S. M. (2001b). A wake-up call from the thalamus. Nat. Neurosci. 4 344–346.
    1. Shimizu V. T., Bueno O. F., Miranda M. C. (2014). Sensory processing abilities of children with ADHD. Brazil. J. Phys. Ther. 18 343–352.
    1. Shiramatsu T. I., Hitsuyu R., Ibayashi K., Kanzaki R., Kawai K., Takahashi H. (2016). Effect of vagus nerve stimulation on neural adaptation in thalamo-cortical system in rats. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. 2016 1834–1837. 10.1109/EMBC.2016.7591076
    1. Sillito A. M., Kemp J. A., Berardi N. (1983). The cholinergic influence on the function of the cat dorsal lateral geniculate nucleus (dLGN). Brain Res. 280 299–307.
    1. Simpson K. L., Altman D. W., Wang L., Kirifides M. L., Lin R. C., Waterhouse B. D. (1997). Lateralization and functional organization of the locus coeruleus projection to the trigeminal somatosensory pathway in rat. J. Comp. Neurol. 385 135–147.
    1. Slater C., Wang Q. (2021). Alzheimer’s disease: an evolving understanding of noradrenergic involvement and the promising future of electroceutical therapies. Clin. Transl. Med. 11:e397. 10.1002/ctm2.397
    1. Sperling W., Biermann T., Spannenberger R., Clepce M., Padberg F., Reulbach U., et al. (2011). Changes in gustatory perceptions of patients with major depression treated with vagus nerve stimulation (VNS). Pharmacopsychiatry 44 67–71. 10.1055/s-0030-1268427
    1. Stanley G. B., Jin J., Wang Y., Desbordes G., Wang Q., Black M. J., et al. (2012). Visual orientation and directional selectivity through thalamic synchrony. J. Neurosci. 32 9073–9088. 10.1523/JNEUROSCI.4968-11.2012
    1. Surowka A. D., Krygowska-Wajs A., Ziomber A., Thor P., Chrobak A. A., Szczerbowska-Boruchowska M. (2015). Peripheral vagus nerve stimulation significantly affects lipid composition and protein secondary structure within dopamine-related brain regions in rats. Neuromol. Med. 17 178–191. 10.1007/s12017-015-8349-7
    1. Sutcliffe P. A., Bishop D. V., Houghton S., Taylor M. (2006). Effect of attentional state on frequency discrimination: a comparison of children with ADHD on and off medication. J. Speech Lang. Hear. Res. 49 1072–1084. 10.1044/1092-4388(2006/076)
    1. Swadlow H. A., Gusev A. G. (2001). The impact of ‘bursting’ thalamic impulses at a neocortical synapse. Nat. Neurosci. 4 402–408. 10.1038/86054
    1. Szczerbowska-Boruchowska M., Krygowska-Wajs A., Ziomber A., Thor P., Wrobel P., Bukowczan M., et al. (2012). The influence of electrical stimulation of vagus nerve on elemental composition of dopamine related brain structures in rats. Neurochem. Int. 61 156–165. 10.1016/j.neuint.2012.04.018
    1. Takahashi H., Shiramatsu T. I., Hitsuyu R., Ibayashi K., Kawai K. (2020). Vagus nerve stimulation (VNS)-induced layer-specific modulation of evoked responses in the sensory cortex of rats. Sci. Rep. 10:8932. 10.1038/s41598-020-65745-z
    1. Thakkar V. J., Engelhart A. S., Khodaparast N., Abadzi H., Centanni T. M. (2020). Transcutaneous auricular vagus nerve stimulation enhances learning of novel letter-sound relationships in adults. Brain Stimul. 13 1813–1820. 10.1016/j.brs.2020.10.012
    1. Trulson M. E., Jacobs B. L. (1979). Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res. 163 135–150.
    1. Tun P. A., Williams V. A., Small B. J., Hafter E. R. (2012). The effects of aging on auditory processing and cognition. Am. J. Audiol. 21 344–350.
    1. Tyler R., Cacace A., Stocking C., Tarver B., Engineer N., Martin J., et al. (2017). Vagus nerve stimulation paired with tones for the treatment of tinnitus: a prospective randomized double-blind controlled pilot study in humans. Sci. Rep. 7:11960. 10.1038/s41598-017-12178-w
    1. Ungless M. A. (2004). Dopamine: the salient issue. Trends Neurosci. 27 702–706.
    1. Van Bockstaele E. J., Peoples J., Telegan P. (1999). Efferent projections of the nucleus of the solitary tract to peri-locus coeruleus dendrites in rat brain: evidence for a monosynaptic pathway. J. Comp. Neurol. 412 410–428. 10.1002/(sici)1096-9861(19990927)412:3<410::aid-cne3>;2-f
    1. Vanneste S., Martin J., Rennaker R. L., II, Kilgard M. P. (2017). Pairing sound with vagus nerve stimulation modulates cortical synchrony and phase coherence in tinnitus: an exploratory retrospective study. Sci. Rep. 7:17345. 10.1038/s41598-017-17750-y
    1. Vazey E. M., Moorman D. E., Aston-Jones G. (2018). Phasic locus coeruleus activity regulates cortical encoding of salience information. Proc. Natl. Acad. Sci. U.S.A. 115 E9439–E9448. 10.1073/pnas.1803716115
    1. Verdier D., Dykes R. W. (2001). Long-term cholinergic enhancement of evoked potentials in rat hindlimb somatosensory cortex displays characteristics of long-term potentiation. Exp. Brain Res. 137 71–82. 10.1007/s002210000646
    1. Videen T. O., Daw N. W., Rader R. K. (1984). The effect of norepinephrine on visual cortical neurons in kittens and adult cats. J. Neurosci. 4 1607–1617.
    1. Vinck M., Batista-Brito R., Knoblich U., Cardin J. A. (2015). Arousal and locomotion make distinct contributions to cortical activity patterns and visual encoding. Neuron 86 740–754. 10.1016/j.neuron.2015.03.028
    1. Wall P. D., Dubner R. (1972). Somatosensory pathways. Annu. Rev. Physiol. 34 315–336.
    1. Wang Q., Millard D. C., Zheng H. J. V., Stanley G. B. (2012). Voltage-sensitive dye imaging reveals improved topographic activation of cortex in response to manipulation of thalamic microstimulation parameters. J. Neural Eng. 9:026008. 10.1088/1741-2560/9/2/026008
    1. Wang Q., Webber R., Stanley G. B. (2010). Thalamic synchrony and the adaptive gating of information flow to cortex. Nat. Neurosci. 13 1534–1541. 10.1038/nn.2670
    1. Waterhouse B. D., Devilbiss D., Seiple S., Markowitz R. (2004). Sensorimotor-related discharge of simultaneously recorded, single neurons in the dorsal raphe nucleus of the awake, unrestrained rat. Brain Res. 1000 183–191. 10.1016/j.brainres.2003.11.030
    1. Waterhouse B. D., Navarra R. L. (2019). The locus coeruleus-norepinephrine system and sensory signal processing: a historical review and current perspectives. Brain Res. 1709 1–15. 10.1016/j.brainres.2018.08.032
    1. Wells M. F., Wimmer R. D., Schmitt L. I., Feng G., Halassa M. M. (2016). Thalamic reticular impairment underlies attention deficit in Ptchd1(Y/-) mice. Nature 532 58–63. 10.1038/nature17427
    1. Weyand T. G., Boudreaux M., Guido W. (2001). Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J. Neurophysiol. 85 1107–1118.
    1. Wiegand I., Tollner T., Dyrholm M., Muller H. J., Bundesen C., Finke K. (2014). Neural correlates of age-related decline and compensation in visual attention capacity. Neurobiol. Aging 35 2161–2173. 10.1016/j.neurobiolaging.2014.02.023
    1. Wilson D. A., Fletcher M. L., Sullivan R. M. (2004). Acetylcholine and olfactory perceptual learning. Learn. Mem. 11 28–34.
    1. Wimmer R. D., Schmitt L. I., Davidson T. J., Nakajima M., Deisseroth K., Halassa M. M. (2015). Thalamic control of sensory selection in divided attention. Nature 526 705–709.
    1. Woolrych A., Vautrelle N., Reynolds J. N. J., Parr-Brownlie L. C. (2021). Throwing open the doors of perception: the role of dopamine in visual processing. Eur. J. Neurosci. 54 6135–6146. 10.1111/ejn.15408
    1. Yakunina N., Kim S. S., Nam E. C. (2018). BOLD fMRI effects of transcutaneous vagus nerve stimulation in patients with chronic tinnitus. PLoS One 13:e0207281. 10.1371/journal.pone.0207281
    1. Zhan X., Yin P., Heinbockel T. (2013). The basal forebrain modulates spontaneous activity of principal cells in the main olfactory bulb of anesthetized mice. Front. Neural Circ. 7:148. 10.3389/fncir.2013.00148
    1. Zhang K., Chen C. D., Monosov I. E. (2019). Novelty, salience, and surprise timing are signaled by neurons in the basal forebrain. Curr. Biol. 29 134.e3–142.e3. 10.1016/j.cub.2018.11.012
    1. Zheng H. J. V., Wang Q., Stanley G. B. (2015). Adaptive shaping of cortical response selectivity in the vibrissa pathway. J. Neurophysiol. 113 3850–3865.
    1. Ziomber A., Thor P., Krygowska-Wajs A., Zalecki T., Moskala M., Romanska I., et al. (2012). Chronic impairment of the vagus nerve function leads to inhibition of dopamine but not serotonin neurons in rat brain structures. Pharmacol. Rep. 64 1359–1367. 10.1016/s1734-1140(12)70933-7

Source: PubMed

3
Sottoscrivi