Enhancement of Attentional Performance by Selective Stimulation of α4β2* nAChRs: Underlying Cholinergic Mechanisms
Open accessAbstract
Impairments in attention are a major component of the cognitive symptoms of neuropsychiatric and neurodegenerative disorders. Using an operant sustained attention task (SAT), including a distractor condition (dSAT), we assessed the putative pro-attentional effects of the selective alpha4beta2(*) nicotinic acetylcholine receptor (nAChR) agonist S 38232 in comparison with the non-selective agonist nicotine. Neither drug benefited SAT performance. However, in interaction with the increased task demands implemented by distractor presentation, the selective agonist, but not nicotine, enhanced the detection of signals during the post-distractor recovery period. This effect is consistent with the hypothesis that second-long increases in cholinergic activity ('transients') mediate the detection of cues and that nAChR agonists augment such transients. Electrochemical recordings of prefrontal cholinergic transients evoked by S 38232 and nicotine indicated that the alpha4beta2(*) nAChR agonist evoked cholinergic transients that were characterized by a faster rise time and more rapid decay than those evoked by nicotine. Blockade of the alpha7 nAChR 'sharpens' nicotine-evoked transients; therefore, we determined the effects of co-administration of nicotine and the alpha7 nAChR antagonist methyllycaconitine on dSAT performance. Compared with vehicle and nicotine alone, this combined treatment significantly enhanced the detection of signals. These results indicate that compared with nicotine, alpha4beta2(*) nAChR agonists significantly enhance attentional performance and that the dSAT represents a useful behavioral screening tool. The combined behavioral and electrochemical evidence supports the hypothesis that nAChR agonist-evoked cholinergic transients, which are characterized by rapid rise time and fast decay, predict robust drug-induced enhancement of attentional performance.
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Stimulation of α4β2 nicotinic receptors in the medial prefrontal cortex enhances performance in a visual attention task.
“stimulation of α4β2 nicotinic receptors in the medial prefrontal cortex enhances performance in a visual attention task (Howe et al., 2010)”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Howe et al., 2010
Some essential features of this circuitry have been validated in terms of predicting the effects of cholinergic drugs on attentional performance.
“Importantly, some essential features of this circuitry have been validated in terms of predicting the effects of cholinergic drugs on attentional performance (Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
Cholinergic stimulation of α4β2* nAChRs evokes cholinergic transients via stimulating glutamate release, and the mediodorsal input is required to generate such transients.
“Furthermore, cholinergic stimulation of α4β2* nAChRs evoked cholinergic transients via stimulating glutamate release, and the mediodorsal input is required to generate such transients.”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
The decay rate of cholinergic transients is not controlled by glutamatergic-cholinergic interactions.
“In contrast to the amplitude of cholinergic transients, the decay rate of such transients, that is, the duration and rate of decrease of ACh release is not controlled by these glutamatergic-cholinergic interactions (Parikh et al, 2008, 2010; Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
The amplitude of cholinergic transients is determined by glutamatergic stimulation of ionotropic glutamate receptors.
“Evidence from neuropharmacological studies using selective nAChR ligands and antagonists at ionotropic glutamate receptors, and assessing the effects of infusions of these compounds into the PFC of animals lacking α4β2* or α7 nAChRs, or animals with lesions of the MD, collectively indicated that the amplitude of cholinergic transients is determined by glutamatergic stimulation of ionotropic”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
Stimulation of α4β2* nAChRs, by administering systemically a full α4β2* nAChR agonist, increased the number of cue detections in SAT performing animals; this effect was seen specifically during performance recovery subsequently to the presentation of a distractor.
“Furthermore, stimulation of α4β2* nAChRs, by administering systemically a full α4β2* nAChR agonist, increased the number of cue detections in SAT performing animals; this effect was seen specifically during performance recovery subsequently to the presentation of a distractor (“dSAT” performance; Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
Co-administration of nicotine and MLA sharpens the cholinergic transients evoked by nicotine.
“Corresponding with the behavioral evidence, this combination treatment also “sharpened” the cholinergic transients evoked by nicotine (Howe et al. 2010)”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al. 2010
The full agonist at α4β2* nAChRs S 38232 is more efficacious in enhancing attentional performance than nicotine.
“Evidence from animal studies on the effects of a full agonist at α4β2* nAChRs, S 38232, confirmed that such compounds are more efficacious in enhancing attentional performance than nicotine (Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
Removing the contribution of α7 nAChRs to the effects of nicotine transforms nicotine into a more efficacious enhancer of attentional performance.
“To the contrary, we find that removing the contribution of these receptors to the effects of nicotine transforms nicotine into a more efficacious enhancer of attentional performance (Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
Stimulation of α4β2* nAChRs amplifies cholinergic transients and enhances attentional performance.
“Most obviously, we can stimulate α4β2* nAChRs to amplify cholinergic transients and enhance attentional performance (e.g., Howe et al, 2010).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Howe et al, 2010
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“In addition, prefrontal 2*-nAChRs are known to be involved in attentional performance (41).”
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“The dSAT offers a variation from the original task, whereby a distracting flashing light is introduced a third of the way through the trials, assessing the animal’s ability to maintain attention during distraction (Howe et al., 2010).”
BackgroundPharmacological Enhancement of Memory and Executive Functioning in Laboratory Animals
Floresco, S., & Jentsch, J. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.158 · Cited by 109 · see citing works
Kramer, P. F., Brill-Weil, S. G., Cummins, A. C., Zhang, R., Camacho-Hernandez, G. A., Newman, A. H., Eldridge, M. A. G., Averbeck, B. B., & Khaliq, Z. M. (2022) · Neuron · doi:10.1016/j.neuron.2022.07.011 · Cited by 104 · see citing works
Deficits in attentional control: Cholinergic mechanisms and circuitry-based treatment approaches.
Sarter, M. F., & Paolone, G. (2011) · Behavioral Neuroscience · doi:10.1037/a0026227 · Cited by 98 · see citing works
The role of nicotinic acetylcholine receptors in autosomal dominant nocturnal frontal lobe epilepsy
Becchetti, A., Aracri, P., Meneghini, S., Brusco, S., & Amadeo, A. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00022 · Cited by 102 · see citing works
Deterministic functions of cortical acetylcholine
Sarter, M. F., Lustig, C., Howe, W. M., Gritton, H. J., & Berry, A. S. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12515 · Cited by 96 · see citing works
“Furthermore, glutamate release from these thalamic inputs is itself modulated by cholinergic activity and stimulation of nAChRs (Gioanni et al., 1999; Lambe et al., 2003; Howe et al., 2010; Parikh et al., 2010).”
Parikh, V., Kutlu, M. G., & Gould, T. J. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.01.020 · Cited by 95 · see citing works
“Moreover, pharmacological stimulation of α4β2 nAChRs by specific ligands facilitated baseline attentional performance and performance under conditions of higher attentional load (Howe et al., 2010; McGaughy et al., 1999; Mohler et al., 2010) while antagonism of these receptors produced deficits in attention and workin…”
BackgroundCognitive Enhancers (Nootropics). Part 1: Drugs Interacting with Receptors
Froestl, W., Muhs, A., & Pfeifer, A. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-121186 · Cited by 91 · see citing works
“ment of age-related cognitive disorders [247, 248]”
Alzheimer's disease and age-related memory decline (preclinical)
Terry, A. V., Callahan, P. M., Hall, B. J., & Webster, S. J. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.02.002 · Cited by 86 · see citing works
“…α2β4 agonist Schneider et al., 2003 ABT-418 α4β2 agonist Prendergast et al., 1998 ABT-594 α4β2 agonist Buccafusco et al., 2007 S-38232 α4β2 agonist Howe et al., 2010 ABT-089 α4β2 partial agonist Decker et al., 1997 Ispronicline/AZD-3480 α4β2 partial agonist Gatto et al.,…”
BackgroundNeural circuits for a top-down control of fear and extinction
Marek, R., Sun, Y., & Sah, P. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5033-2 · Cited by 86 · see citing works
Cognitive correlates of α4β2 nicotinic acetylcholine receptors in mild Alzheimer’s dementia
Sabri, O., Meyer, P., Graef, S., Hesse, S., Wilke, S., Becker, G., Rullmann, M., Patt, M., Luthardt, J., Wagenknecht, G., et al. (2018) · Brain · doi:10.1093/brain/awy099 · Cited by 87 · see citing works
“The PET findings support the view that fronto-thalamic-striatal a4b2nAChRs contribute to the functional cholinergic network of attention (Sarter et al., 2001; Howe et al., 2010).”
ResultSarter, M. F., Lustig, C., & Taylor, S. F. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.12.001 · Cited by 82 · see citing works
“In our experiments, the beneficial attentional effects of nicotine were statistically robust when its effects at the α7 nAChR were blocked (Howe et al., 2010).”
InfluentialKucinski, A. J., Paolone, G., Bradshaw, M., Albin, R. L., & Sarter, M. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2545-13.2013 · Cited by 81 · see citing works
“Nicotinic drugs have been demonstrated to benefit SAT performance (Howe et al., 2010) and, thus, in interaction with potentially relatively low doses of L-DOPA, may benefit the nonmotor symptoms of PD (Schneider et al., 1998, 1999, 2003; Decamp and Schneider, 2009).”
BackgroundMechanisms Generating Dual-Component Nicotinic EPSCs in Cortical Interneurons
Bennett, C., Arroyo, S., Berns, D. S., & Hestrin, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3565-12.2012 · Cited by 80 · see citing works
“…(BF) activate nicotinic acetylcholine receptors (nAChRs) throughout the cortex and play an important role in sensory processing (Metherate and Hsieh, 2004; Disney et al., 2007), attention (Howe et al., 2010), and learning (Gu and Yakel, 2011; Letzkus et al., 2011; for review see Levin, 2002).”
BackgroundRole of neuronal nicotinic acetylcholine receptors (nAChRs) on learning and memory in zebrafish
Braida, D., Ponzoni, L., Martucci, R., Sparatore, F., Gotti, C., & Sala, M. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3340-1 · Cited by 78 · see citing works
“Both the α4β2 and the α7 subtypes have received a great deal of attention as important drug targets for cognitive enhancement (Hahn et al. 2003; Bitner et al. 2007; Howe et al. 2010; Castner et al. 2011; Lendvai et al. 2013).”
BackgroundInfluentialLeveraging the cortical cholinergic system to enhance attention
Demeter, E., & Sarter, M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.060 · Cited by 75 · see citing works
“In awake animals performing the SAT, systemic injection of a α4β2* agonist also results in cholinergic transients with higher amplitudes and sharper, faster decay profiles than injections of nicotine, confirming the patterns seen in anesthetized animals (Howe et al., 2010).”
BackgroundMethodInfluentialThe role of acetylcholine in negative encoding bias: Too much of a good thing?
Mineur, Y. S., & Picciotto, M. R. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14641 · Cited by 78 · see citing works
“Mechanisms underlying attention rely heavily on the activity of several nAChR subtypes (Howe et al., 2010), as was confirmed by studies conducted knockout mice. β2containing nAChRs in cortico-thalamic projections decrease auditory discrimination (Horst et al., 2012; Howe et al., 2010; Parikh, Ji,…”
BackgroundResultInfluentialAlterations in α4β2 nicotinic receptors in cognitive decline in Alzheimer’s aetiopathology
Okada, H., Ouchi, Y., Ogawa, M., Futatsubashi, M., Saito, Y., Yoshikawa, E., Terada, T., Oboshi, Y., Tsukada, H., Ueki, T., et al. (2013) · Brain · doi:10.1093/brain/awt195 · Cited by 72 · see citing works
Young, J. W., Meves, J. M., & Geyer, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.028 · Cited by 69 · see citing works
Kolisnyk, B., Al‐Onaizi, M., Hirata, P. H. F., Guzmán, M. S., Nikolova, S., Barbash, S., Soreq, H., Bartha, R., Prado, M. A. M., & Prado, V. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1933-13.2013 · Cited by 67 · see citing works
Effects of chronic low- and high-dose nicotine on cognitive flexibility in C57BL/6J mice
Ortega, L. A., Tracy, B. A., Gould, T., & Parikh, V. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.032 · Cited by 67 · see citing works
Nicotine addiction and psychiatric disorders
Kutlu, M. G., Parikh, V., & Gould, T. J. (2015) · International Review of Neurobiology · doi:10.1016/bs.irn.2015.08.004 · Cited by 65 · see citing works
“In an operant sustained attention task, neither nicotine nor an α4β2 nAChR agonist, S38232, was effective but when a distractor cue was added, S38232 enhanced attention (Howe et al., 2010).”
BackgroundSelf-citationNicotinic modulation of cortical circuits
Arroyo, S., Bennett, C., & Hestrin, S. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00030 · Cited by 64 · see citing works
Cholinergic double duty: cue detection and attentional control
Sarter, M., & Lustig, C. (2019) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2018.12.026 · Cited by 64 · see citing works
Self-citationNicotine improves performance in an attentional set shifting task in rats
Allison, C., & Shoaib, M. C. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.055 · Cited by 59 · see citing works
Proulx, É., Piva, M., Tian, M. K., Bailey, C. D. C., & Lambe, E. K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1481-3 · Cited by 57 · see citing works
Hahn, B., Shoaib, M. C., & Stolerman, I. P. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2258-8 · Cited by 59 · see citing works
“The recent finding that MLA sharpened nicotine-induced transient increases in medial prefrontal acetylcholine release and helped unmask attention-enhancing effects of nicotine on a measure of stimulus detection (Howe et al. 2010) points towards previously unexplored functions of cortical α7 nAChRs.”
BackgroundGrupe, M., Grunnet, M., Bastlund, J. F., & Jensen, A. A. (2014) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.12361 · Cited by 54 · see citing works
Rezvani, A. H., Cauley, M., Sexton, H., Xiao, Y., Brown, M. L., Paige, M. A., McDowell, B. E., Kellar, K. J., & Levin, E. D. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2161-8 · Cited by 50 · see citing works
Prefrontal neuromodulation by nicotinic receptors for cognitive processes
Coura, R., & Granon, S. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2596-6 · Cited by 51 · see citing works
Slater, C. L., Liu, Y., Weiss, E., Yu, K., & Wang, Q. (2022) · Brain Sciences · doi:10.3390/brainsci12070890 · Cited by 49 · see citing works
Barak, S., & Weiner, I. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.03.011 · Cited by 50 · see citing works
“Nicotine (acute 0.025–0.75 mg/kg or chronic 5 mg/kg/day) , given on its own did not improve, and even impaired, SAT performance in normal rats (Bushnell et al., 1997; Howe et al., 2010; Rezvani and Levin, 2004, 2003b).”
BackgroundInfluentialPoorthuis, R. B., & Mansvelder, H. D. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.003 · Cited by 48 · see citing works
“literature on cholinergic control of attention; readers are referred to excellent recent reviews [31,34–37].”
BackgroundPieramico, V., Esposito, R., Cesinaro, S., Frazzini, V., & Sensi, S. L. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00153 · Cited by 48 · see citing works
“Selective α4β2 nicotinic receptor agonists represent a new class of drugs acting on the cholinergic system and found to induce attentional and cognitive improvements in animal models (Howe et al., 2010).”
BackgroundEffect of ADHD medication in male C57BL/6J mice performing the rodent Continuous Performance Test
Caballero-Puntiverio, M., Lerdrup, L., Grupe, M., Larsen, C., Dietz, A. G., & Andreasen, J. T. (2019) · Psychopharmacology · doi:10.1007/s00213-019-5167-x · Cited by 48 · see citing works
Vandesquille, M., Baudonnat, M., Decorte, L., Louis, C., Lestage, P. J., & Béracochéa, D. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.10.006 · Cited by 46 · see citing works
“, nicotine, acetylcholine) (Howe et al., 2010; Parikh et al., 2008; 2010).”
BackgroundSarter, M. F., Lustig, C., Blakely, R., & Cherian, A. K. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.07.001 · Cited by 46 · see citing works
“…hypothesized that the higher levels of cholinergic neuromodulation increases the likelihood and amplitude of cholinergic transients, thereby enhancing cue 4 detection performance during or after distractor challenges (Howe et al., 2010; Parikh et al., 2010; Parikh and Sarter, 2008; Sarter, 2015).”
InfluentialGould, R. W., Garg, P., Garg, S., & Nader, M. A. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.004 · Cited by 44 · see citing works
“…within the mammalian CNS are α7 and α4β2* receptors and subtype-selective agonists at each subtype have produced cognitive enhancing effects in animal models (e.g., Hahn et al., 2003; Bitner et al., 2007; Howe et al., 2010; Castner et al., 2011) and may have lower abuse liability than nicotine.”
BackgroundDiminished trk A receptor signaling reveals cholinergic‐attentional vulnerability of aging
Parikh, V., Howe, W. M., Welchko, R. M., Naughton, S. X., D'Amore, D. E., Han, D. J., Deo, M., Turner, D. L., & Sarter, M. F. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12090 · Cited by 45 · see citing works
“AAV-trkA reduces prefrontal ACh release capacity in aged rats Brief, second-based release of ACh in medial prefrontal cortex mediates the detection of signals in attentional tasks (Parikh et al., 2007; Parikh & Sarter, 2008; Howe et al., 2010; Hasselmo & Sarter, 2011).”
BackgroundThe Role of Nicotine in Schizophrenia
Featherstone, R. E., & Siegel, S. J. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.07.002 · Cited by 46 · see citing works
Kim, K., Müller, M. L. T. M., Bohnen, N. I., Sarter, M. F., & Lustig, C. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.02.006 · Cited by 46 · see citing works
“…this increased engagement is more strongly associated with attempts to recover performance after it has been impaired by the challenge than the ability to maintain it (e.g., Demeter et al., 2011; Berry et al., 2015, in revision; Howe et al., 2010; Kozak et al., 2006; 2007; Parikh et al., 2013).”
Cholinergic Signaling Dynamics and Cognitive Control of Attention
Parikh, V., & Bangasser, D. A. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_133 · Cited by 42 · see citing works
Louth, E. L., Bignell, W., Taylor, C. L., & Bailey, C. D. C. (2016) · eNeuro · doi:10.1523/eneuro.0267-16.2016 · Cited by 40 · see citing works
Nicotinic ligands as multifunctional agents for the treatment of neuropsychiatric disorders
Terry, A. V., Callahan, P. M., & Hernandez, C. M. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.07.027 · Cited by 40 · see citing works
“, 5-choice serial reaction time task (5C-SRTT) [26, 80, 82, 83, 84, 85, 90] and visual signal detection task [81, 86 178]) measuring attentional and impulsivity processes in laboratory animals.”
Nicotinic acetylcholine receptor ligands, a patent review (2006 – 2011)
Gündisch, D., & Eibl, C. (2011) · Expert Opinion on Therapeutic Patents · doi:10.1517/13543776.2011.637919 · Cited by 39 · see citing works
Mineur, Y. S., & Picciotto, M. R. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15943 · Cited by 38 · see citing works
Maloku, E., Kadriu, B., Zhubi, A., Dong, E., Pibiri, F., Satta, R., & Guidotti, A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.21 · Cited by 37 · see citing works
Peters, M. S., Cherian, A. K., Bradshaw, M., & Sarter, M. F. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.025 · Cited by 38 · see citing works
Organization of the Basal Forebrain Cholinergic Projection System
Záborszky, L., Duque, A., Gielow, M. R., Gombkötő, P., Nádasdy, Z., & Somogyi, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00019-x · Cited by 38 · see citing works
“The effect of ACh released through BF cholinergic axons in the cortex is complex due to: (1) the differential regional and laminar distribution of cholinergic axons; (2) different effects on various neuronal types and cellular sites of action (cell bodies, dendrites, axons); (3) ACh effects are mediated by synaptic an…”
McClernon, F. J., Froeliger, B., Rose, J. E., Kozink, R. V., Addicott, M. A., Sweitzer, M. M., Westman, E. C., & Wert, D. M. V. (2015) · Addiction Biology · doi:10.1111/adb.12253 · Cited by 37 · see citing works
“…research with rodents and non-human primates suggests that nicotine decreases the influence of distractors on task performance (Hahn, Shoaib & Stolerman 2002; Bain et al. 2003) and that this effect is mediated via the α4β2 nicotine receptor system (Prendergast et al. 1998; Howe et al. 2010).”
BackgroundYoung, J. W., Kamenski, M. E., Higa, K. K., Light, G. A., Geyer, M. A., & Zhou, X. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.120 · Cited by 36 · see citing works
“As reported for humans and rats (Demeter et al , 2013; Howe et al , 2010), we demonstrated that the attentional performance of mice was deleteriously affected by distracting stimuli (trial period 2, cf. trial periods 1 and 3; Figure 2a and i).”
Simulation of cholinergic and noradrenergic modulation of behavior in uncertain environments
Avery, M. C., Nitz, D. A., Chiba, A. A., & Krichmar, J. L. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00005 · Cited by 36 · see citing works
“Specifically, studies have shown that cholinergic inputs to PFC are important for cue detection and attention (Parikh and Sarter, 2008; Howe et al., 2010).”
BackgroundInfluentialAttention and the Cholinergic System: Relevance to Schizophrenia
Lustig, C., & Sarter, M. F. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_5009 · Cited by 34 · see citing works
Dehydroepiandrosterone, its metabolites and ion channels
Hill, M., Dušková, M., & Stárka, L. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.05.006 · Cited by 33 · see citing works
“The steroid sensitive 4 2* nAChR influence learning and attenional performance [10,22] and the 4 2* subunits are also known o participate in the stimulation of dopamine release in nucleus ccumbens, which influence the alcohol, drug and tobacco addicion [23].”
BackgroundMar, A. C., Nilsson, S. R. O., Gamallo‐Lana, B., Lei, M., Dourado, T., Alsiö, J., Saksida, L. M., Bussey, T. J., & Robbins, T. W. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4679-5 · Cited by 33 · see citing works
“Improvements in response accuracy, total correct, and speeded correct reaction times have also been observed under specific conditions within the 5-CSRTT and SAT/dSAT paradigms following α4β2nAChR agonist treatment (McGaughy et al. 1999; Mohler et al. 2010; Howe et al. 2010).”
BackgroundNicotinic Receptors and Attention
Hahn, B. (2015) · Current topics in behavioral neurosciences · doi:10.1007/978-3-319-13665-3_5 · Cited by 32 · see citing works
Chen, Q., Yang, L., Li, D., Zhai, J., Jiang, W., & Xie, X. (2020) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2020.128836 · Cited by 32 · see citing works
Grupe, M., Jensen, A. A., Ahring, P. K., Christensen, J., & Grunnet, M. (2012) · British Journal of Pharmacology · doi:10.1111/bph.12095 · Cited by 32 · see citing works
“It has been demonstrated that transient increases in ACh in prefrontal cortex (at the scale of seconds) is necessary for cue detection in a rat attention task (Parikh et al., 2007), involving especially a4b2 nAChRs (Parikh et al., 2008; Howe et al., 2010).”
BackgroundPaolone, G., Lee, T. M., & Sarter, M. F. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2271-12.2012 · Cited by 32 · see citing works
“…cholinergic activity upregulates the interactions between cue-evoked thalamic glutamatergic and a separate, phasic component of cholinergic neurotransmission, thereby increasing the probability of hits in attention tasks (Parikh et al., 2007, 2008; Howe et al., 2010; Hasselmo and Sarter, 2011).”
BackgroundBehavioral-cognitive targets for cholinergic enhancement
Sarter, M. F. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.004 · Cited by 29 · see citing works
Lenz, R. A., Pritchett, Y., Berry, S. M., Llano, D. A., Han, S., Berry, D. A., Sadowsky, C., Abi‐Saab, W., & Saltarelli, M. D. (2015) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0000000000000093 · Cited by 28 · see citing works
Caldirola, D., Daccò, S., Grassi, M., Citterio, A., Menotti, R., Cavedini, P., Girardi, P., & Perna, G. (2013) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.12m07985 · Cited by 27 · see citing works
Aracri, P., Amadeo, A., Pasini, M. E., Fascio, U., & Becchetti, A. (2013) · Synapse · doi:10.1002/syn.21655 · Cited by 27 · see citing works
“The prominent role of the latter is increasingly recognized (e.g., Bailey et al., 2010; Guillem et al., 2011; Hahn et al., 2003; Howe et al., 2010), and stimulation of nAChRs is being considered for cognitive enhancing therapy in neurodegenerative P.”
BackgroundBehavioral Animal Models to Assess Pro-cognitive Treatments for Schizophrenia
Young, J. W., Amitai, N., & Geyer, M. A. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25758-2_3 · Cited by 26 · see citing works
Cole, R. D., Poole, R. L., Guzman, D. M., Gould, T. J., & Parikh, V. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3754-4 · Cited by 24 · see citing works
“This interpretation is supported by the idea that activation of α4β2 nAChRs supports top-down attentional processes and not performance under conditions requiring lower attentional demands (Howe et al. 2010; Sarter and Paolone 2011; Demeter and Sarter 2013).”
InfluentialJučaitė, A., Öhd, J., Potter, A., Jaeger, J., Karlsson, P., Hannesdóttir, K., Boström, E., NEWHOUSE, P. A., & Paulsson, B. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3116-7 · Cited by 25 · see citing works
“Selective agonists for α4β2* nAChRs have been shown to enhance sustained attention performance, to improve vigilance in rodents, to prevent distractibility and improve accuracy in non-human primates (Prendergast et al. 1998; McGaughy et al. 1999; Grottick et al. 2001; Howe et al. 2010; Rezvani et al. 2011, 2012; Young…”
BackgroundPaolone, G., Mallory, C. S., Cherian, A. K., Miller, T. R., Blakely, R., & Sarter, M. F. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.07.032 · Cited by 24 · see citing works
“Our evidence and the derived circuitry model suggest that cholinergic activity modulates cortical target circuitry primarily via a4b2* nAChRs (Parikh et al., 2010; Howe et al., 2010; Hasselmo and Sarter, 2011).”
BackgroundNeuronal effects of nicotine during auditory selective attention
Smucny, J., D, A. O. M., Eichman, L. C., & Tregellas, J. R. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3832-7 · Cited by 22 · see citing works
“2002) and nicotinic receptor subtype-specific agonists (Howe et al. 2010).”
Whole-brain modeling explains the context-dependent effects of cholinergic neuromodulation
Coronel‐Oliveros, C., Gießing, C., Medel, V., Cofré, R., & Orio, P. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119782 · Cited by 22 · see citing works
Hahn, B., Shrieves, M. E., Olmstead, C. K., Yuille, M. B., Chiappelli, J., Pereira, E. F. R., Albuquerque, E. X., & Fawcett, W. P. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05363-4 · Cited by 22 · see citing works
Rezvani, A. H., Cauley, M. C., Johnson, E. C., Gatto, G. J., & Levin, E. D. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2712-2 · Cited by 21 · see citing works
“…nicotinic agonists enhance cognitive performance in experimental animals (Buccafusco and Terry 2009; Hahn and Stolerman 2002; Hahn et al. 2011; Howe et al. 2010; Levin et al. 2006; Mirza and Stolerman 2000; Rezvani et al. 2011; Sarter et al. 2009; Young et al. 2004) and humans (Levin et al.…”
Grupe, M., Paolone, G., Jensen, A. A., Sandager‐Nielsen, K., Sarter, M. F., & Grunnet, M. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.09.005 · Cited by 21 · see citing works
“Interestingly, local ejections of α4β2* preferring agonists into the mPFC evoke ‘sharp’ neurotransmitter transients similar to those observed in performing animals [7, 8, 12].”
BackgroundGrupe, M., Grunnet, M., Laursen, B., & Bastlund, J. F. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.12.008 · Cited by 20 · see citing works
Azimi, M., Oemisch, M., & Womelsdorf, T. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05430-w · Cited by 19 · see citing works
“Among nonhuman primate studies using alpha-4/beta-2 agonists, there has been no demonstration of specific attention effects (Buccafusco et al. 1995; Buccafusco et al. 2007; Decamp and Schneider 2006; Decker et al. 1997; Gould et al. 2013; Howe et al. 2010; Kolisnyk et al. 2015; Paolone et al. 2013; Prendergast et al.…”
BackgroundMethodInfluentialNicotine reduces distraction under low perceptual load
Behler, O., Breckel, T. P. K., & Thiel, C. M. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3761-5 · Cited by 19 · see citing works
Callahan, P. M., & Terry, A. V. (2015) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-16522-6_5 · Cited by 19 · see citing works
Xanomeline restores endogenous nicotinic acetylcholine receptor signaling in mouse prefrontal cortex
Power, S. K., Venkatesan, S., & Lambe, E. K. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01531-5 · Cited by 17 · see citing works
Laikowski, M. M., Reisdorfer, F., & Moura, S. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180410105135 · Cited by 17 · see citing works
- Authors
- Howe, W. M., Ji, J., Parikh, V., Williams, S., Mocaër, E., Trocmé-Thibierge, C., & Sarter, M.
- Affiliations
- University of Michigan (US)
- Temple University (US)
- Servier (France) (FR)
- Corresponding author
- Sarter, Martin
- Venue
- Neuropsychopharmacology
- Published
- 2010-02-10
- Volume
- 35
- Issue
- 6
- Pages
- 1391-1401
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC2855755
- OpenAlex
- W2085190125
- Cited by
- 150
- References
- 48
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 4 · 2021: 3 · 2020: 7 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 10 · 2015: 14 · 2014: 16 · 2013: 22 · 2012: 22
- FWCI
- 9.13
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Servier
- Institut de Recherches Servier
- National Institute of Mental Health (R01MH080332, R21MH080426, MH080426, MH 080332)
- National Institute on Drug Abuse (T32DA007267)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- attention, nicotinic acetylcholine receptors, nicotine, alpha7 nAChR, methyllycaconitine, sustained attention, distractor task, prefrontal cortex, electrochemical recording, attentional enhancement
- MeSH terms
- Acetylcholine, Animals, Attention, Brain, Brain Chemistry, Cognition, Cues, Drug Interactions, Male, Neuropsychological Tests, Nicotine, Psychomotor Performance, Receptors, Nicotinic, Rats, Wistar, Prefrontal Cortex, Nicotinic Agonists, Nicotinic Antagonists, Excitatory Postsynaptic Potentials, Rats, Electrochemical Techniques, Executive Function, alpha7 Nicotinic Acetylcholine Receptor
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