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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
Abstract
Rats were trained in a previously validated behavioral vigilance task that required them to detect visual signals of variable length and to discriminate signal from nonsignal events. Baseline performance was characterized by a signal length-dependent ability to score hits, a decline in hits over time, and a correct rejection rate of approximately 70%. After the rats reached criterion performance in this task, the immunotoxin 192 IgG-saporin or its vehicle was infused into the area of the nucleus basalis/substantia innominata of the basal forebrain. Postoperative performance in lesioned rats was characterized by a decrease in their ability to detect signals while their ability to correctly reject nonsignals remained unaffected. The effect of the lesion did not recover in the course of over 180 sessions of postlesion testing. The overall performance of the rats correlated with acetylcholinesterase (AChE)-positive fiber density in all cortical areas measured except the cingulate and pyriform cortex. These findings help to elucidate the nature of the attentional impairments resulting from the loss of cortical cholinergic inputs.
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“In rodents, lesions of cholinergic inputs to the cortex impair tests of sustained attention, particularly across sensory modalities (McGaughy et al., 2002; McGaughy et al., 1996; Turchi and Sarter, 1997).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as McGaughy et al., 1996
In the citing paper
“At the same time, this deafferentation did not affect the animals’ response accuracy in blank trials (i.e., the correct reporting of the absence of a cue).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as McGaughy et al, 1996
In the citing paper
“While intact animals detected over 70–80% of the longest (500 ms) cues, cortical cholinergic deafferentation reduced the detection rate for all cues to about 30%, with no recovery despite several months of daily post-surgery practice (McGaughy et al, 1996).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as McGaughy et al, 1996
In the citing paper
“Removal of cortical cholinergic inputs selectively and persistently impaired the animals’ detection rate (or number of hits). In contrast, response accuracy in blank trials remained completely spared.”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as McGaughy et al, 1996
In the citing paper
“As orienting is not necessary for detection, the residual hit rate following cortical cholinergic deafferentation (McGaughy et al, 1996) may have been due to detections that occurred without the facilitating benefits of attentional orienting.”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as McGaughy et al, 1996
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Butt, A. E., & Bowman, T. D. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4013 · Cited by 30
“A wide range of such attention-demanding tasks have revealed impairments following 192 IgG‐saporin lesions of the NBM (e.g., Baxter et al., 1995; Chiba, Bucci, Holland, & Gallagher, 1995; McGaughy, Decker, & Sarter, 1999; McGaughy, Kaiser, & Sarter, 1996; McGaughy & Sarter, 1998; Turchi & Sarter, 1997; Waite, Wardlow,…”
Orexin A-induced enhancement of attentional processing in rats: role of basal forebrain neurons
Zajo, K. N., Fadel, J. R., & Burk, J. A. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4139-z · Cited by 29
“SAT was calculated using the following formula: SAT=((H−FA)/ (2×(H+FA)−(H+FA)2) ) (Boschen et al. 2009;McGaughy et al. 1996).”
BackgroundMethodInfluentialBehavioral-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
Self-citationMartínez, V., & Sarter, M. F. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301661 · Cited by 29
“…(2008) 33, 2635–2647 & 2008 Nature Publishing Group All rights reserved 0893-133X/08 $30.00 www.neuropsychopharmacology.org system and evokes significant increases in cortical acetylcholine (ACh) release (Arnold et al, 2002; Kozak et al, 2006; McGaughy et al, 1996; McGaughy and Sarter, 1998).”
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“Tasks that place specific demands on attention appear to be sensitive to NBM lesions, mainly those assessing operant measures of sustained attention (McGaughy et al. 1996, 2002; Robbins 2002), and also selective attention tasks (Muir et al. 1992) or divided attention paradigms (Turchi and Sarter…”
Influence of benzodiazepine binding site ligands on fear-conditioned contextual memory
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“Consistent with evidence indicating that cholinergic signaling is essential for the detection of cues in attentional contexts (McGaughy et al., 1996; Dalley et al., 2004; St Peters et al., 2011; Gritton et al., 2016; Sarter et al., 2016; Berry et al., 2017; Howe et al., 2017; Kim et al., 2019; Sarter and Lustig, 2020)…”
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“Performance of behavioral vigilance tasks by rats has revealed that impairment in the task was correlated with the loss of acetylcholinesterase (AChE)fiber density (McGaughy et al. 1996).”
BackgroundButt, A. E., & Hodge, G. K. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00062-4 · Cited by 25
Fadel, J. R., Sarter, M. F., & Bruno, J. P. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00515-6 · Cited by 27
Self-citationBehavioral 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
Adenosine inhibits glutamatergic input to basal forebrain cholinergic neurons
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“In addition, BF cholinergic neurons are known to modulate complex functions of vigilance including sensory processing and cognitive performances, involving both attentional and learning processes (McGaughy et al. 1996; Sarter and Bruno 1997; Sarter et al. 1999; Semba 2000).”
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“…tasks designed to assess attention in animals, this laboratory and others have demonstrated the necessity of basal forebrain activation and cortical cholinergic transmission for attentional processing (Muir et al., 1994, 1995; McGaughy et al., 1996; McGaughy & Sarter, 1998; Turchi & Sarter, 2001).”
BackgroundSelf-citationLack of effect of moderate Purkinje cell loss on working memory
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“SAT performance is mediated by, and requires, increases in prefrontal ACh release (Kozak et al., 2006, 2007; St Peters et al., 2011b; McGaughy et al., 1996).”
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“rons likely being primarily responsible for the decrease in hits (McGaughy et al., 1996).”
BackgroundSelf-citationStress Regulation of Sustained Attention and the Cholinergic Attention System
Eck, S. R., Xu, S., Telenson, A. M., Duggan, M. R., Cole, R. D., Wicks, B., Bergmann, J., Lefebo, H., Shore, M. E., Shepard, K. A., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.04.013 · Cited by 26
“Lesions and optogenetic suppression of NBM cholinergic neurons disrupt performance on signaled trials, while optogenetic stimulation of these neurons enhances performance on signaled trials(11, 12).”
BackgroundLower plasma choline levels are associated with sleepiness symptoms
Pak, V. M., Dai, F., Keenan, B. T., Gooneratne, N. S., & Pack, A. I. (2017) · Sleep Medicine · doi:10.1016/j.sleep.2017.10.004 · Cited by 25
“In another experiment, infusions of the cholinotoxin 192 IgG-saporin induced loss of cortical cholinergic inputs, which resulted in rats’ impaired performance in a sustained attention test, while performance on non-attention related control activities remained unaffected (54).”
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The role of the medial prefrontal cortex in attention: Altering predictability of task difficulty
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Make a Left Turn: Cortico‐Striatal Circuitry Mediating the Attentional Control of Complex Movements
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Self-citationAlexander, K., Brooks, J. M., Sarter, M. F., & Bruno, J. P. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.105 · Cited by 21
“Removal of cholinergic inputs to the cortex causes persistent impairments in attentional performance, assessed by a range of tasks (e.g., McGaughy et al., 1996 e.g., McGaughy et al., 2002).”
Self-citationPotential roles of cholinergic modulation in the neural coding of location and movement speed
Dannenberg, H., Hinman, J. R., & Hasselmo, M. E. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.09.002 · Cited by 22
“Selective saporin lesions of cholinergic innervation of the prefrontal cortex have been shown to impair sustained attention for the detection of brief visual cues (McGaughy et al., 1996; McGaughy and Sarter, 1998).”
BackgroundLü, Y., Sarter, M. F., Żochowski, M., & Booth, V. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14744 · Cited by 20
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“In contrast, these neurons do seem to be required for modulation of attentional processing (Baxter, Gallagher, & Holland, 1999; Baxter, Holland, & Gallagher, 1997; Chiba, Bucci, Holland, & Gallagher, 1995; Mc-Gaughy, Dalley, Morrison, Everitt, & Robbins, 2002; McGaughy, Kaiser, & Sarter, 1996; Waite, Wardlow, & Power,…”
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Himmelheber, A. M., Bruno, J. P., & Sarter, M. F. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00266-7 · Cited by 19
Self-citationVisuospatial task-related prefrontal activity is correlated with negative symptoms in schizophrenia
Curtin, A., Sun, J., Zhao, Q., Onaral, B., Wang, J., Tong, S., & Ayaz, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-45893-7 · Cited by 18
Lesions of the rat nucleus basalis magnocellularis disrupt appetitive-to-aversive transfer learning
Butt, A. E., Schultz, J. A., Arnold, L. L., Garman, E., George, C. L., & Garraghty, P. E. (2003) · Integrative Psychological and Behavioral Science · doi:10.1007/bf02688857 · Cited by 18
“Behavioral tasks showing sensitivity to SAP lesions of the NBM include tests of incremental attention in Pavlovian conditioning paradigms (Baxter et al., 1995; Chiba et al., 1995), operant measures of sustained attention or vigilance (McGaughy et al., 1999; McGaughy et al., 1996; McGaughy & Sarter, 1998), selective at…”
MethodCraft, T. K. S., Mahoney, J. H., DeVries, A. C., & Sarter, M. F. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04136.x · Cited by 18
“This pattern of impairment precisely mirrors the effects of immunotoxin-induced loss of cortical cholinergic inputs (McGaughy et al., 1996; McGaughy & Sarter, 1998).”
BackgroundInfluentialSelf-citationButt, A. E., Noble, M. M., Rogers, J. L., et al. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.2.241 · Cited by 18
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“We plan to assess PPTg lesioned rats' performance on an attention task where failure to detect a visual signal requires a lever press response, rather than a response omission [ 12 ,42].”
InfluentialEvaluation of muscarinic and nicotinic receptor antagonists on attention and working memory
McQuail, J. A., & Burk, J. A. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.11.015 · Cited by 16
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Self-citationPosterior parietal cortex dynamically ranks topographic signals via cholinergic influence
Broussard, J. I. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00032 · Cited by 19
“Loss of BFCS input to the cortex impairs performance in both the 5CSRTT (Muir et al., 1994) and the SAT (McGaughy et al., 1996; Bushnell et al., 1998; Chiba et al., 1999).”
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Yegla, B., & Parikh, V. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.042 · Cited by 16
“…inputs is necessary for normal attentional performance, and that such performance robustly activates cortical acetylcholine (ACh) release (McGaughy et al., 1996; Everitt and Robbins, 1997; Passetti et al., 2000; Arnold et al., 2002; Dalley et al., 2004; Sarter and Parikh, 2005; Parikh et…”
BackgroundResultSarter, M. F., Bruno, J. P., Parikh, V., Martínez, V., Kozak, R., & Richards, J. B. (2006) · Birkhäuser Basel eBooks · doi:10.1007/978-3-7643-7772-4_4 · Cited by 17
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Findings about the Cholinergic Basal Forebrain Using Immunotoxin to the Nerve Growth Factor Receptor
Wiley, R. G. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48615.x · Cited by 15
Ultrastructural evidence for mu-opioid modulation of cholinergic pathways in rat dentate gyrus
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“The integrity of the forebrain cholinergic system is critical for an array of high integrative processes, which include development and plasticity of cortical representations, mechanisms of attention and memory formation (McGaughy et al., 1996; Sarter et al., 2005).”
BackgroundKucinski, A. J., Avila, C., & Sarter, M. F. (2022) · eNeuro · doi:10.1523/eneuro.0418-22.2022 · Cited by 12
“…for understanding the time-on-task decrement seen in STs. Early studies on the effects of basal forebrain cholinergic lesions on hit rates (McGaughy et al., 1996), trial-specific recordings of cholinergic activity and associated oscillatory activity (Parikh et al., 2007; Howe et al.,…”
BackgroundMethodSelf-citationNeonatal 192 IgG-saporin lesion of forebrain cholinergic neurons: focus on the life span?
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Effects of 192 IgG-saporin on acetylcholinesterase histochemistry in male and female rats
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“It has also been shown that performance, in a task incorporating components of selective and sustained attention, is disrupted by excitotoxic lesions of the basal forebrain (McGaughy and Sarter, 1998; McGaughy et al., 1996; Muir et al., 1994, 1995).”
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“…this sustained attention task have demonstrated that immunotoxic lesions of the corticopetal cholinergic neurons in the basal forebrain (e.g., McGaughy et al., 1996) result in a selective impairment in the ability of rats to detect visual signals (hits), while leaving the ability to…”
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“These observations are consistent with other studies demonstrating a role for NB cholinergic neurons in the ability to sustain or shift attention (McGaughy et al., 1996; McGaughy et al., 2002; Lehmann et al., 2003).”
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Self-citationMemory and the septo-hippocampal system
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A search for residual behavioral effects of trichloroethylene (TCE) in rats exposed as young adults
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Touchscreen Sustained Attention Task (SAT) for Rats
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α5 nAChR modulation of the prefrontal cortex makes attention resilient
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Attentional demands for demonstrating deficits following intrabasalis infusions of 192 IgG-saporin
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Self-citationThe effects of ongoing distraction on the neural processes underlying signal detection
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“The SAT and dSAT paradigm has been used extensively in animal model studies of the neurobiological mechanisms underlying attentional functions (e.g., Gritton et al., 2016; Kozak et al., 2006; McGaughy et al., 1996; St Peters et al., 2011a, 2011b).”
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“This assertion is consistent with the role of nbm corticopetal cholinergic neurons in attentional processing (Baxter et al., 1999; McGaughy et al., 1996; Sarter and Bruno, 1997) and data that demonstrates nbm corticopetal cholinergic lesions do not induce general deficits in anxiety-like states.”
ResultA theory of the septo-hippocampal system
Gray, J. A., & McNaughton, N. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198522713.003.0010 · Cited by 8
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Postnatal ethanol exposure disrupts signal detection in adult rats
Woolfrey, K. M., Hunt, P. S., & Burk, J. A. (2005) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2005.07.002 · Cited by 6
Hupalo, S., Spencer, R. C., & Berridge, C. W. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15260 · Cited by 6
“The current study utilized male animals in part to align with a large body of work describing the neurobiology underlying sustained attention in males (Aston- Jones et al., 1999; McGaughy et al., 1996; Sarter et al., 2001; Spencer & Berridge, 2019).”
ResultCase, J. L., Arruda, J. E., & VanWormer, L. A. (2016) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2016.01.006 · Cited by 6
Cherian, A. K., Tronson, N. C., Parikh, V., Kucinski, A. J., Blakely, R., & Sarter, M. F. (2019) · Behavioral Neuroscience · doi:10.1037/bne0000310 · Cited by 7
Self-citationA theory of the behavioural inhibition system
Gray, J. A., & McNaughton, N. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198522713.003.0005 · Cited by 6
Garg, R., Qiu, Q., & Yu, C. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003374 · Cited by 5
Orexins and Cognition: Neuroanatomical and Neurochemical Substrates
Burk, J. A., Maness, E. B., Blumenthal, S. A., & Fadel, J. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813751-2.00007-3 · Cited by 4
Robinson, A. M., Mangini, D. F., & Burk, J. A. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111415732 · Cited by 5
“Overall, this pattern of impairment is similar to the deficits observed following widespread loss of corticopetal cholinergic neurons (McGaughy and Sarter, 1998; McGaughy et al., 1996), suggesting that muscarinic M1 receptors in multiple cortical regions may contribute to attentional performance (Sarter et al.”
BackgroundResultSalm, A. K., Lally, B. E., Borysiewicz, E., Fil, D., & Konat, G. W. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.027 · Cited by 6
Howe, W. M., & Burk, J. A. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.08.037 · Cited by 4
Tsolias, A., Zhou, Y., Mojica, C. A., Sakharkar, M., Tsolias, M., Moore, T. L., Rosene, D. L., & Medalla, M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0953-23.2024 · Cited by 3
Neurotoxic Effects, Mechanisms, and Outcome of 192 IgG-Saporin Lesions
Petrosini, L., Bartolo, P. D., & Cutuli, D. (2022) · Springer eBooks · doi:10.1007/978-3-031-15080-7_79 · Cited by 3
Dietary choline supplementation in adult rats improves performance on a test of recognition memory
Moreno, H. C., Hall, G., Gallo, M., & de Brugada, I. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.04.030 · Cited by 3
Parikh, V., & Sarter, M. F. (2013) · Neuromethods · doi:10.1007/978-1-62703-370-1_12 · Cited by 3
Self-citationCortico-Striatal, Cognitive-Motor Interactions Underlying Complex Movement Control Deficits
Kucinski, A. J., & Sarter, M. F. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-3-319-42743-0_6 · Cited by 3
Self-citationBeselia, G. V., Chkhikvishvili, N. C., Burjanadze, M. A., et al. (2021) · Neuroreport · doi:10.1097/wnr.0000000000001671 · Cited by 3
Metadata
- Authors
- McGaughy, J., Kaiser, T., & Sarter, M.
- Affiliations
- The Ohio State University (US)
- Venue
- Behavioral Neuroscience
- Published
- 1996-04
- Volume
- 110
- Issue
- 2
- Pages
- 247-265
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W2075076974
- Cited by
- 435
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 28 · 2022: 7 · 2021: 5 · 2020: 7 · 2019: 8 · 2018: 8 · 2017: 8 · 2016: 17 · 2015: 13 · 2014: 15 · 2013: 15 · 2012: 16
- FWCI
- 6.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ag010173-10)
- National Institute on Aging (AG10 173)
- National Institute of Mental Health (MH01072, K02MH001072)
- National Institute of Neurological Disorders and Stroke (NS32938, R01NS032938)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Pharmacology (medical) › Cholinesterase and Neurodegenerative Diseases
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- 192 IgG-saporin, nucleus basalis of Meynert, substantia innominata, basal forebrain, attentional impairment, signal detection, visual discrimination, lesion recovery, rats
- MeSH terms
- Saporins, Acetylcholinesterase, Animals, Antibodies, Monoclonal, Immunotoxins, Attention, Brain Mapping, Carbolines, Cerebral Cortex, Cholinergic Fibers, Conditioning, Operant, Discrimination Learning, Male, N-Glycosyl Hydrolases, Rats, Inbred F344, Mental Recall, Substantia Innominata, Visual Perception, Prosencephalon, Cholinergic Agents, Rats, Ribosome Inactivating Proteins, Type 1
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