Skip to main content

Cholinergic Signaling Dynamics and Cognitive Control of Attention

Part of the Current Topics in Behavioral Neurosciences book series (CTBN,volume 45)

Abstract

The central cholinergic system is one of the most important modulator neurotransmitter system implicated in diverse behavioral processes. Activation of the basal forebrain cortical cholinergic input system represents a critical step in cortical information processing. This chapter explores recent developments illustrating cortical cholinergic transmission mediate defined cognitive operations, which is contrary to the traditional view that acetylcholine acts as a slowly acting neuromodulator that influences arousal cortex-wide. Specifically, we review the evidence that phasic cholinergic signaling in the prefrontal cortex is a causal mediator of signal detection. In addition, studies that support the neuromodulatory role of cholinergic inputs in top-down attentional control are summarized. Finally, we review new findings that reveal sex differences and hormonal regulation of the cholinergic-attention system.

Keywords

  • Acetylcholine
  • Attention
  • Muscarinic receptors
  • Nicotinic receptors
  • Sex differences

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/7854_2020_133
  • Chapter length: 17 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   149.00
Price excludes VAT (USA)
  • ISBN: 978-3-030-56013-3
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   199.99
Price excludes VAT (USA)
Hardcover Book
USD   199.99
Price excludes VAT (USA)

References

  • Allison C, Shoaib M (2013) Nicotine improves performance in an attentional set shifting task in rats. Neuropharmacology 64:314–320

    CAS  PubMed  Google Scholar 

  • Apparsundaram S, Martinez V, Parikh V, Kozak R, Sarter M (2005) Increased capacity and density of choline transporters situated in synaptic membranes of the right medial prefrontal cortex of attentional task-performing rats. J Neurosci 25:3851–3856

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold HM, Burk JA, Hodgson EM, Sarter M, Bruno JP (2002) Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience 114:451–460

    CAS  PubMed  Google Scholar 

  • Ballinger EC, Ananth M, Talmage DA, Role LW (2016) Basal forebrain cholinergic circuits and signaling in cognition and cognitive decline. Neuron 91:1199–1218

    CAS  CrossRef  Google Scholar 

  • Bangasser DA, Wicks B, Waxler DE, Eck SR (2017) Touchscreen sustained attention task (SAT) for rats. J Vis Exp 127:e56219

    Google Scholar 

  • Barnes P, Staal V, Muir J, Good MA (2006) 17-β estradiol administration attenuates deficits in sustained and divided attention in young ovariectomized rats and aged acyclic female rats. Behav Neurosci 120:1225–1234

    CAS  PubMed  Google Scholar 

  • Bartolini A, Pepeu G (1967) Investigations into the acetylcholine output from the cerebral cortex of the cat in the presence of hyoscine. Br J Pharmacol Chemother 31:66–73

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995) Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109:714–722

    CAS  PubMed  Google Scholar 

  • Bayless DW, Darling JS, Stout WJ, Daniel JM (2012) Sex differences in attentional processes in adult rats as measured by performance on the 5-choice serial reaction time task. Behav Brain Res 235:48–54

    PubMed  Google Scholar 

  • Berry AS, Blakely RD, Sarter M, Lustig C (2015) Cholinergic capacity mediates prefrontal engagement during challenges to attention: evidence from imaging genetics. NeuroImage 108:386–395

    CAS  PubMed  Google Scholar 

  • Berry AS, Sarter M, Lustig C (2017) Distinct frontoparietal networks underlying attentional effort and cognitive control. J Cogn Neurosci 29:1212–1225

    PubMed  PubMed Central  Google Scholar 

  • Bortz DM, Mikkelsen JD, Bruno JP (2013) Localized infusions of the partial alpha 7 nicotinic receptor agonist SSR180711 evoke rapid and transient increases in prefrontal glutamate release. Neuroscience 255:55–67

    CAS  PubMed  Google Scholar 

  • Botly LC, De Rosa E (2009) Cholinergic deafferentation of the neocortex using 192 IgG-saporin impairs feature binding in rats. J Neurosci 29:4120–4130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buhusi M, Bartlett MJ, Buhusi CV (2017) Sex differences in interval timing and attention to time in C57Bl/6J mice. Behav Brain Res 324:96–99

    PubMed  PubMed Central  Google Scholar 

  • Callahan MJ, Kinsora JJ, Harbaugh RE, Reeder TM, Davis RE (1993) Continuous ICV infusion of scopolamine impairs sustained attention of rhesus monkeys. Neurobiol Aging 14:147–151

    CAS  PubMed  Google Scholar 

  • Chudasama Y, Dalley JW, Nathwani F, Bouger P, Robbins TW (2004) Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem 11:78–86

    PubMed  PubMed Central  Google Scholar 

  • Cole RD, Kawasumi Y, Parikh V, Bangasser DA (2016) Corticotropin releasing factor impairs sustained attention in male and female rats. Behav Brain Res 296:30–34

    CAS  PubMed  Google Scholar 

  • Cosgrove KP, Esterlis I, McKee SA et al (2012) Sex differences in availability of β2∗-nicotinic acetylcholine receptors in recently abstinent tobacco smokers. Arch Gen Psychiatry 69:418–427

    CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis L, Buisson B, Bertrand S, Bertrand D (2002) Potentiation of human α4β2 neuronal nicotinic acetylcholine receptor by estradiol. Mol Pharmacol 61:127

    CAS  PubMed  Google Scholar 

  • Dalley JW, McGaughy J, O'Connell MT, Cardinal RN, Levita L, Robbins TW (2001) Distinct changes in cortical acetylcholine and noradrenaline efflux during contingent and noncontingent performance of a visual attentional task. J Neurosci 21:4908–4914

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dalley JW, Theobald DE, Bouger P, Chudasama Y, Cardinal RN, Robbins TW (2004) Cortical cholinergic function and deficits in visual attentional performance in rats following 192 IgG-saporin-induced lesions of the medial prefrontal cortex. Cereb Cortex 14:922–932

    PubMed  Google Scholar 

  • Dasari S, Hill C, Gulledge AT (2017) A unifying hypothesis for M1 muscarinic receptor signalling in pyramidal neurons. J Physiol 595:1711–1723

    CAS  PubMed  Google Scholar 

  • Demeter E, Sarter M, Lustig C (2008) Rats and humans paying attention: cross-species task development for translational research. Neuropsychology 22:787–799

    PubMed  PubMed Central  Google Scholar 

  • Demeter E, Hernandez-Garcia L, Sarter M, Lustig C (2011) Challenges to attention: a continuous arterial spin labeling (ASL) study of the effects of distraction on sustained attention. NeuroImage 54:1518–1529

    PubMed  Google Scholar 

  • Descarries L (1998) The hypothesis of an ambient level of acetylcholine in the central nervous system. J Physiol Paris 92:215–220

    CAS  PubMed  Google Scholar 

  • Ferguson SM, Blakely RD (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol Interv 4:22–37

    CAS  PubMed  Google Scholar 

  • Frick KM, Kim JJ, Baxter MG (2004) Effects of complete immunotoxin lesions of the cholinergic basal forebrain on fear conditioning and spatial learning. Hippocampus 14:244–254

    CAS  PubMed  Google Scholar 

  • Gao S, Hendrie HC, Hall KS, Hui S (1998) The relationships between age, sex, and the incidence of dementia and Alzheimer disease: a meta-analysis. Arch Gen Psychiatry 55:809–815

    CAS  PubMed  Google Scholar 

  • Gibbs RB (1996) Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res 720:61–68

    CAS  PubMed  Google Scholar 

  • Gibbs RB (1997) Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res 757:10–16

    CAS  PubMed  Google Scholar 

  • Gibbs RB, Wu D, Hersh LB, Pfaff DW (1994) Effects of estrogen replacement on the relative levels of choline Acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol 129:70–80

    CAS  PubMed  Google Scholar 

  • Giuliano C, Parikh V, Ward JR, Chiamulera C, Sarter M (2008) Increases in cholinergic neurotransmission measured by using choline-sensitive microelectrodes: enhanced detection by hydrolysis of acetylcholine on recording sites? Neurochem Int 52:1343–1350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein JM, Seidman LJ, Goodman JM, Koren D, Lee H et al (1998) Are there sex differences in neuropsychological functions among patients with schizophrenia? Am J Psychiatr 155:1358–1364

    CAS  PubMed  Google Scholar 

  • Gotti C, Clementi F, Fornari A, Gaimarri A, Guiducci S et al (2009) Structural and functional diversity of native brain neuronal nicotinic receptors. Biochem Pharmacol 78:703–711

    CAS  PubMed  Google Scholar 

  • Gritton HJ, Howe WM, Mallory CS, Hetrick VL, Berke JD, Sarter M (2016) Cortical cholinergic signaling controls the detection of cues. Proc Natl Acad Sci U S A 113:E1089–E1097

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME, Sarter M (2011) Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36:52–73

    CAS  PubMed  Google Scholar 

  • Himmelheber AM, Sarter M, Bruno JP (1997) Operant performance and cortical acetylcholine release: role of response rate, reward density, and non-contingent stimuli. Brain Res Cogn Brain Res 6:23–36

    CAS  PubMed  Google Scholar 

  • Howe WM, Ji J, Parikh V, Williams S, Mocaer E et al (2010) Enhancement of attentional performance by selective stimulation of alpha4beta2(∗) nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology 35:1391–1401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Howe WM, Berry AS, Francois J, Gilmour G, Carp JM et al (2013) Prefrontal cholinergic mechanisms instigating shifts from monitoring for cues to cue-guided performance: converging electrochemical and fMRI evidence from rats and humans. J Neurosci 33:8742–8752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Howe WM, Gritton HJ, Lusk NA, Roberts EA, Hetrick VL et al (2017) Acetylcholine release in prefrontal cortex promotes gamma oscillations and theta-gamma coupling during cue detection. J Neurosci 37:3215–3230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jentsch JD, Taylor JR (2003) Sex-related differences in spatial divided attention and motor impulsivity in rats. Behav Neurosci 117:76–83

    PubMed  Google Scholar 

  • Kozak R, Bruno JP, Sarter M (2006) Augmented prefrontal acetylcholine release during challenged attentional performance. Cereb Cortex 16:9–17

    PubMed  Google Scholar 

  • Lambe EK, Picciotto MR, Aghajanian GK (2003) Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28:216–225

    CAS  PubMed  Google Scholar 

  • Lean GA, Liu YJ, Lyon DC (2019) Cell type specific tracing of the subcortical input to primary visual cortex from the basal forebrain. J Comp Neurol 527:589–599

    PubMed  Google Scholar 

  • Lucas-Meunier E, Monier C, Amar M, Baux G, Fregnac Y, Fossier P (2009) Involvement of nicotinic and muscarinic receptors in the endogenous cholinergic modulation of the balance between excitation and inhibition in the young rat visual cortex. Cereb Cortex 19:2411–2427

    PubMed  Google Scholar 

  • Maddux JM, Kerfoot EC, Chatterjee S, Holland PC (2007) Dissociation of attention in learning and action: effects of lesions of the amygdala central nucleus, medial prefrontal cortex, and posterior parietal cortex. Behav Neurosci 121:63–79

    PubMed  PubMed Central  Google Scholar 

  • Mazure CM, Swendsen J (2016) Sex differences in Alzheimer’s disease and other dementias. Lancet Neurol 15:451–452

    PubMed  PubMed Central  Google Scholar 

  • McGaughy J, Sarter M (1999) Effects of ovariectomy, 192 IgG-saporin-induced cortical cholinergic deafferentation, and administration of estradiol on sustained attention performance in rats. Behav Neurosci 113:1216–1232

    CAS  PubMed  Google Scholar 

  • McGaughy J, Kaiser T, Sarter M (1996) Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 110:247–265

    CAS  PubMed  Google Scholar 

  • McGaughy J, Everitt BJ, Robbins TW, Sarter M (2000) The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav Brain Res 115:251–263

    CAS  PubMed  Google Scholar 

  • Mendrek A, Mancini-Marïe A (2016) Sex/gender differences in the brain and cognition in schizophrenia. Neurosci Biobehav Rev 67:57–78

    PubMed  Google Scholar 

  • Mesulam M (2004) The cholinergic lesion of Alzheimer’s disease: pivotal factor or side show? Learn Mem 11:43–49

    PubMed  Google Scholar 

  • Mielke MM, Vemuri P, Rocca WA (2014) Clinical epidemiology of Alzheimer’s disease: assessing sex and gender differences. Clin Epidemiol 6:37–48

    PubMed  PubMed Central  Google Scholar 

  • Miettinen RA, Kalesnykas G, Koivisto EH (2002) Estimation of the total number of cholinergic neurons containing estrogen receptor-alpha in the rat basal forebrain. J Histochem Cytochem 50:891–902

    CAS  PubMed  Google Scholar 

  • Nakamura N, Fujita H, Kawata M (2002) Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 109:473–485

    CAS  PubMed  Google Scholar 

  • Newhouse PA, Potter A, Singh A (2004) Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4:36–46

    CAS  PubMed  Google Scholar 

  • Newman LA, McGaughy J (2008) Cholinergic deafferentation of prefrontal cortex increases sensitivity to cross-modal distractors during a sustained attention task. J Neurosci 28:2642–2650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Norbury R, Travis MJ, Erlandsson K, Waddington W, Ell PJ, Murphy DGM (2007) Estrogen therapy and brain muscarinic receptor density in healthy females: a SPET study. Horm Behav 51:249–257

    CAS  PubMed  Google Scholar 

  • Paolone G, Angelakos CC, Meyer PJ, Robinson TE, Sarter M (2013) Cholinergic control over attention in rats prone to attribute incentive salience to reward cues. J Neurosci 33:8321–8335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parikh V, Sarter M (2008) Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity. Ann N Y Acad Sci 1129:225–235

    CAS  PubMed  Google Scholar 

  • Parikh V, Pomerleau F, Huettl P, Gerhardt GA, Sarter M, Bruno JP (2004) Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur J Neurosci 20:1545–1554

    PubMed  Google Scholar 

  • Parikh V, Kozak R, Martinez V, Sarter M (2007) Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56:141–154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parikh V, Man K, Decker MW, Sarter M (2008) Glutamatergic contributions to nicotinic acetylcholine receptor agonist-evoked cholinergic transients in the prefrontal cortex. J Neurosci 28:3769–3780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parikh V, Ji J, Decker MW, Sarter M (2010) Prefrontal beta2 subunit-containing and alpha7 nicotinic acetylcholine receptors differentially control glutamatergic and cholinergic signaling. J Neurosci 30:3518–3530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parikh V, St Peters M, Blakely RD, Sarter M (2013) The presynaptic choline transporter imposes limits on sustained cortical acetylcholine release and attention. J Neurosci 33:2326–2337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Passetti F, Dalley JW, O’Connell MT, Everitt BJ, Robbins TW (2000) Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur J Neurosci 12:3051–3058

    CAS  PubMed  Google Scholar 

  • Pepeu G, Giovannini MG (2009) Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6:86–96

    CAS  PubMed  Google Scholar 

  • Phillis JW (1968) Acetylcholine release from the cerebral cortex: its role in cortical arousal. Brain Res 7:378–389

    CAS  PubMed  Google Scholar 

  • Posner MI, Snyder CR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol 109:160–174

    CAS  PubMed  Google Scholar 

  • Ramtekkar UP, Reiersen AM, Todorov AA, Todd RD (2010) Sex and age differences in attention-deficit/hyperactivity disorder symptoms and diagnoses: implications for DSM-V and ICD-11. J Am Acad Child Adolesc Psychiatry 49:217–28e1–3

    PubMed  PubMed Central  Google Scholar 

  • Rocca WA, Grossardt BR, Shuster LT (2011) Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res 1379:188–198

    CAS  PubMed  Google Scholar 

  • Sarter M, Kim Y (2015) Interpreting chemical neurotransmission in vivo: techniques, time scales, and theories. ACS Chem Neurosci 6:8–10

    CAS  PubMed  Google Scholar 

  • Sarter M, Lustig C (2019) Cholinergic double duty: cue detection and attentional control. Curr Opin Psychol 29:102–107

    PubMed  Google Scholar 

  • Sarter M, Parikh V (2005) Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 6:48–56

    CAS  PubMed  Google Scholar 

  • Sarter M, Hasselmo ME, Bruno JP, Givens B (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res Brain Res Rev 48:98–111

    CAS  PubMed  Google Scholar 

  • Sarter M, Gehring WJ, Kozak R (2006) More attention must be paid: the neurobiology of attentional effort. Brain Res Rev 51:145–160

    PubMed  Google Scholar 

  • Sarter M, Paolone G (2011) Deficits in attentional control: cholinergic mechanisms and circuitry-based approaches. Behav Neurosci 125:825–835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarter M, Parikh V, Howe WM (2009a) nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78:658–667

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarter M, Parikh V, Howe WM (2009b) Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci 10:383–390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarter M, Lustig C, Taylor SF (2012) Cholinergic contributions to the cognitive symptoms of schizophrenia and the viability of cholinergic treatments. Neuropharmacology 62:1544–1553

    CAS  PubMed  Google Scholar 

  • Sarter M, Lustig C, Howe WM, Gritton H, Berry AS (2014) Deterministic functions of cortical acetylcholine. Eur J Neurosci 39:1912–1920

    PubMed  PubMed Central  Google Scholar 

  • Sarter M, Lustig C, Berry AS, Gritton H, Howe WM, Parikh V (2016) What do phasic cholinergic signals do? Neurobiol Learn Mem 130:135–141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seçer I, Yılmazoğulları Y (2016) Are attentional resources a mediator for sex differences in memory? Int J Psychol 51:117–122

    PubMed  Google Scholar 

  • St Peters M, Demeter E, Lustig C, Bruno JP, Sarter M (2011) Enhanced control of attention by stimulating mesolimbic-corticopetal cholinergic circuitry. J Neurosci 31:9760–9771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stoet G, O’Connor DB, Conner M, Laws KR (2013) Are women better than men at multi-tasking? BMC Psychol 1:18

    Google Scholar 

  • Stolerman IP, Mirza NR, Hahn B, Shoaib M (2000) Nicotine in an animal model of attention. Eur J Pharmacol 393:147–154

    CAS  PubMed  Google Scholar 

  • Takase K, Mitsushima D, Funabashi T, Kimura F (2007) Sex difference in the 24-h acetylcholine release profile in the premotor/supplementary motor area of behaving rats. Brain Res 1154:105–115

    CAS  PubMed  Google Scholar 

  • Takase K, Kimura F, Yagami T, Mitsushima D (2009) Sex-specific 24-h acetylcholine release profile in the medial prefrontal cortex: simultaneous measurement of spontaneous locomotor activity in behaving rats. Neuroscience 159:7–15

    CAS  PubMed  Google Scholar 

  • Thiele A (2013) Muscarinic signaling in the brain. Annu Rev Neurosci 36:271–294

    CAS  PubMed  Google Scholar 

  • Tinkler GP, Voytko ML (2005) Estrogen modulates cognitive and cholinergic processes in surgically menopausal monkeys. Prog Neuro-Psychopharmacol Biol Psychiatry 29:423–431

    CAS  Google Scholar 

  • Turchi J, Sarter M (1997) Cortical acetylcholine and processing capacity: effects of cortical cholinergic deafferentation on crossmodal divided attention in rats. Brain Res Cogn Brain Res 6:147–158

    CAS  PubMed  Google Scholar 

  • Unal CT, Golowasch JP, Zaborszky L (2012) Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front Behav Neurosci 6:21

    CAS  PubMed  PubMed Central  Google Scholar 

  • van Huizen F, March D, Cynader MS, Shaw C (1994) Muscarinic receptor characteristics and regulation in rat cerebral cortex: changes during development, aging and the oestrous cycle. Eur J Neurosci 6:237–243

    PubMed  Google Scholar 

  • Vuckovich JA, Semel ME, Baxter MG (2004) Extensive lesions of cholinergic basal forebrain neurons do not impair spatial working memory. Learn Mem 11:87–94

    PubMed  PubMed Central  Google Scholar 

  • Weickert TW, Weinberg D, Lenroot R, Catts SV, Wells R et al (2015) Adjunctive raloxifene treatment improves attention and memory in men and women with schizophrenia. Mol Psychiatry 20:685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitmer RA, Quesenberry CP, Zhou J, Yaffe K (2011) Timing of hormone therapy and dementia: the critical window theory revisited. Ann Neurol 69:163–169

    PubMed  Google Scholar 

  • Wiersielis KR, Wicks B, Simko H, Cohen SR, Khantsis S et al (2016) Sex differences in corticotropin releasing factor-evoked behavior and activated networks. Psychoneuroendocrinology 73:204–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilens TE, Decker MW (2007) Neuronal nicotinic receptor agonists for the treatment of attention-deficit/hyperactivity disorder: focus on cognition. Biochem Pharmacol 74:1212–1223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Kuwabara Y, Sasaki M, Fukumura T, Ichimiya A et al (2000) Sex-related differences in the muscarinic acetylcholinergic receptor in the healthy human brain--a positron emission tomography study. Ann Nucl Med 14:97–101

    CAS  PubMed  Google Scholar 

  • Young JW, Geyer MA, Rissling AJ, Sharp RF, Eyler LT et al (2013) Reverse translation of the rodent 5C-CPT reveals that the impaired attention of people with schizophrenia is similar to scopolamine-induced deficits in mice. Transl Psychiatry 3:e324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zaborszky L, Csordas A, Mosca K, Kim J, Gielow MR et al (2015) Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb Cortex 25:118–137

    PubMed  Google Scholar 

  • Zaborszky L, Gombkoto P, Varsanyi P, Gielow MR, Poe G et al (2018) Specific basal forebrain-cortical cholinergic circuits coordinate cognitive operations. J Neurosci 38:9446–9458

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XY, Chen DC, Xiu MH, Yang FD, Haile CN et al (2012) Gender differences in never-medicated first-episode schizophrenia and medicated chronic schizophrenia patients. J Clin Psychiatry 73:1025–1033

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors’ research is supported by grants from the National Institute on Aging (AG046580) to VP and National Science Foundation (NSF CAREER IOS-15524) to DAB.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vinay Parikh .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Verify currency and authenticity via CrossMark

Cite this chapter

Parikh, V., Bangasser, D.A. (2020). Cholinergic Signaling Dynamics and Cognitive Control of Attention. In: Shoaib, M., Wallace, T. (eds) Behavioral Pharmacology of the Cholinergic System. Current Topics in Behavioral Neurosciences, vol 45. Springer, Cham. https://doi.org/10.1007/7854_2020_133

Download citation