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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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“The former is well established to cause impairments in attention (McGaughy et al., 1996; Turchi and Sarter, 2000; Dalley et al., 2004; Botly and De Rosa, 2009), whereas the latter interferes with the execution of repetitive, automated action patterns (Graybiel, 2008; Redgrave et al., 2010).”
BackgroundInfluentialSelf-citationWaite, J. J., Wardlow, M. L., & Power, A. E. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3884 · Cited by 80
Bidirectional interactions between circadian entrainment and cognitive performancePreprint
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BackgroundInfluentialSelf-citationThe role of basal forebrain cholinergic neurons in fear and extinction memory
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Leveraging the cortical cholinergic system to enhance attention
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“…model studies, selective lesions to the basal forebrain cortical cholinergic system in attention task-performing animals result in a severe and lasting impairment in signal detection, while the ability to correctly reject nonsignals remains intact (McGaughy et al., 1996; McGaughy & Sarter, 1998).”
BackgroundInfluentialSelf-citationThe uncertainty processing theory of motivation
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BackgroundMethodResultInfluentialSelf-citationWhat do phasic cholinergic signals do?
Sarter, M. F., Lustig, C., Berry, A. S., Gritton, H. J., Howe, W. M., & Parikh, V. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.02.008 · Cited by 75
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Self-citationAnimal cognition: defining the issues
Sarter, M. F. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.005 · Cited by 72
Self-citationNewman, L. A., & McGaughy, J. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5112-07.2008 · Cited by 71
“Histolog- ical assessment of fiber loss was made using a modified grid counting procedure (McGaughy et al., 1996; Ross et al., 2005).”
BackgroundMethodInfluentialSelf-citationLesions of the basal forebrain impair reversal learning but not shifting of attentional set in rats
Tait, D. S., & Brown, V. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.035 · Cited by 70
The septo-hippocampal system, learning and recovery of function
Niewiadomska, G., Baksalerska-Pazera, M., & Riedel, G. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.03.039 · Cited by 67
“Cortical acetylcholine efflux is critical for attention (Chiba et al., 1995; Dalley et al., 2001; Everitt and Robbins, 1997; McGaughy et al., 1996, 2002; Mesulam, 1990; Sarter and Bruno, 1997; 2000; Sarter et al., 1999, 2001; Voytko, 1996) and has an important role to play in signal-driven versus…”
Frick, K. M., Kim, J. J., & Baxter, M. G. (2004) · Hippocampus · doi:10.1002/hipo.10169 · Cited by 69
“KEY WORDS: 192-IgG saporin; acetylcholine; hippocampus; neocortex; Morris water maze INTRODUCTION Basal forebrain (BF) cholinergic neurons have been regarded as critical to the acquisition of hippocampal- and cortical-dependent information, such as spatial memories.”
BackgroundA review of the 5-Choice Serial Reaction Time (5-CSRT) task in different vertebrate models
Fizet, J., Cassel, J., Kelche, C. R., & Meunier, H. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.027 · Cited by 69
Himmelheber, A. M., Sarter, M., & Bruno, J. P. (1997) · Cognitive Brain Research · doi:10.1016/s0926-6410(97)00014-1 · Cited by 68
Self-citationMaddux, J.-M., Kerfoot, E. C., Chatterjee, S., & Holland, P. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.63 · Cited by 67
“Likewise, McGaughy, Kaiser, and Sarter (1996) found impairments in a signal detection task in rats with selective cholinergic basal forebrain lesions made with 192IgGsaporin.”
BackgroundApparsundaram, S., Martínez, V., Parikh, V., Kozak, R., & Sarter, M. F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0205-05.2005 · Cited by 66
“Past experiments demonstrated that the integrity of cortical cholinergic inputs is necessary for attentional performance (McGaughy et al., 1996).”
Self-citationCholinergic 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
“Correct rejection rates (CRs; correct responses on non-cued trials; see Figure 1 legend for a detailed description of SAT response categories) were not affected, indicating that the impairments were specific to cue detection and not a general performance decline [5].”
BackgroundSelf-citationNicotine 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
Boschen, K. E., Fadel, J. R., & Burk, J. A. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1596-2 · Cited by 66
“A measure of overall SAT accuracy was also calculated using the formula: SAT = (H − FA)/(2 × (H + FA) − (H + FA) 2 ) (McGaughy et al. 1996; Nuechterlein et al. 2009).”
InfluentialSarter, M. F., & Bruno, J. P. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)86039-1 · Cited by 62
Self-citationDringenberg, H. C., Hamze, B., Wilson, A. L., Speechley, W. J., & Kuo, M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk038 · Cited by 66
Bushnell, P. J., & Rice, D. C. (1999) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(99)00006-9 · Cited by 64
Parikh, V., & Sarter, M. F. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03766.x · Cited by 63
“the frontoparietal cortex was quantified using a grid counting technique as described earlier (McGaughy et al. 1996; Burk et al. 2002) using a Leica DM 4000B digital microscope (Nuhsbaum, McHenry, IL, USA).”
MethodSelf-citationDistinct roles of basal forebrain cholinergic neurons in spatial and object recognition memory
Okada, K., Nishizawa, K., Kobayashi, T., Sakata, S., & Kobayashi, K. (2015) · Scientific Reports · doi:10.1038/srep13158 · Cited by 59
Allosteric activators of muscarinic receptors as novel approaches for treatment of CNS disorders
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Ferman, T. J., & Boeve, B. F. (2007) · Neurologic Clinics · doi:10.1016/j.ncl.2007.03.001 · Cited by 68
The Amygdala and Basal Forebrain as a Pathway for Motivationally Guided Attention
Peck, C. J., & Salzman, C. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2106-14.2014 · Cited by 62
“BF lesions cause attentional impairments (Voytko et al., 1994; McGaughy et al., 1996) and alter cortical neuron activity normally modulated by attention (Broussard et al., 2009).”
BackgroundPerry, T., Hodges, H. M., & Gray, J. A. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00413-5 · Cited by 61
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 66
“impairments on attention tasks [27, 28].”
Nicotine improves performance in an attentional set shifting task in rats
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Mattinson, C. E., Burmeister, J. J., Quintero, J. E., Pomerleau, F., Huettl, P. F., & Gerhardt, G. A. (2011) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2011.08.020 · Cited by 57
“…has been shown to result in deficits in spatial working memory (Bailey and Mair, 2005; Romanides et al., 1999), passive avoidance tasks (Torres et al., 1994), and attention (McGaughy et al., 1996), highlighting the importance of these neurotransmitter systems in daily cognitive functioning.”
BackgroundTraissard, N., Herbeaux, K., Cosquer, B., Jeltsch‐David, H., Ferry, B., Galani, R., Pernon, A., Majchrzak, M. J., & Cassel, J. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301116 · Cited by 58
Nicotine–antipsychotic drug interactions and attentional performance in female rats
Rezvani, A. H., & Levin, E. D. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.12.021 · Cited by 59
Vale-Martı́nez, A., Baxter, M. G., & Eichenbaum, H. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02153.x · Cited by 58
“Nevertheless, several reports suggest that the NBM may have a central role in attention and that previous behavioural de®cits seen following NBM lesions may be due to attentional disturbances (Muir et al., 1994; McGaughy et al., 1996; Baxter et al., 1997; McGaughy & Sarter, 1998).”
BackgroundInfluentialTurchi, J. N., & Sarter, M. F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00089-6 · Cited by 56
Self-citationAtomoxetine facilitates attentional set shifting in adolescent rats
Cain, R. E., Wasserman, M. C., Waterhouse, B. D., & McGaughy, J. A. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.04.003 · Cited by 55
Self-citationAttention-modulating effects of cognitive enhancers
Levin, E. D., Bushnell, P. J., & Rezvani, A. H. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.02.008 · Cited by 54
“Partial loss of these cortical cholinergic inputs induced by infusion of 192 IgG-saporin into the basal forebrain of rats decreased the relative number of hits while the relative number of correct rejections (and false alarms) remained unaffected (McGaughy et al., 1996), suggesting that cholinergic input to the cortex…”
Fundamentals of the septo-hippocampal system
Gray, J. A., & McNaughton, N. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198522713.003.0009 · Cited by 66
Parikh, V., Peters, M. S., Blakely, R., & Sarter, M. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4993-12.2013 · Cited by 53
Self-citationCholinergic optimization of cue‐evoked parietal activity during challenged attentional performance
Broussard, J. I., Karelina, K., Sarter, M. F., & Givens, B. S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06713.x · Cited by 53
Self-citationKozak, R., Martínez, V., Young, D. A., Brown, H. D., Bruno, J. P., & Sarter, M. F. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301352 · Cited by 55
“This finding is consistent with the selective impairment in signal trial performance observed following removal of the cortical cholinergic input system (McGaughy et al, 1996).”
ResultSelf-citationLinster, C., Maloney, M. E., Patil, M. M., & Hasselmo, M. E. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00078-9 · Cited by 56
“Selective lesions of cholinergic innervation cause decreases in perceptual discriminability (Linster, Garcia, Hasselmo, & Baxter, 2001) and impairments in continuous performance tasks ( McGaughy, Kaiser, & Sarter, 1996; McGaughy & Sarter, 1998).”
BackgroundNMDA and dopamine interactions in the nucleus accumbens modulate cortical acetylcholine release
Zmarowski, A., Sarter, M., & Bruno, J. P. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04333.x · Cited by 52
“Selective lesions of cholinergic inputs to cortex impair the performance of tasks that explicitly tax sustained and visuo-spatial attention in laboratory animals (McGaughy et al., 1996; Dalley et al., 2004b).”
BackgroundSelf-citationModulation of cognitive processes by transsynaptic activation of the basal forebrain
Givens, B. S., & Sarter, M. F. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(96)00146-5 · Cited by 52
Self-citationBarak, S., & Weiner, I. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.03.011 · Cited by 51
“Similarly, AChE inhibitors failed to improve SAT performance in normal or cholinergically lesioned rats (McGaughy et al., 1999, 1996; McGaughy and Sarter, 1998).”
BackgroundRomberg, C., Bussey, T. J., & Saksida, L. M. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.02.007 · Cited by 49
“007 IgG-saporin lesions of the basal forebrain lead to an increase in correct signal detection errors, while the number of correct rejections remained unchanged [60,63].”
BackgroundPoorthuis, R. B., & Mansvelder, H. D. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.003 · Cited by 54
“involved in sustained attention and cue detection [21–24] and the ability to divide attention between stimuli from different”
BackgroundHarder, J. A., Baker, H. F., & Ridley, R. M. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00381-x · Cited by 49
“, [10,35]) did find an effect on signal detection and vigilance, it might be supposed that failure of a broad function such as attention, in which it has been suggested the NBM plays a major role [40], would produce impairments in the performance of a wide range of tasks [38].”
BackgroundCombined 192 IgG-saporin and 5,7-dihydroxytryptamine lesions in the male rat brain
Lehmann, O., Jeltsch‐David, H., Lazarus, C., et al. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00752-9 · Cited by 48
Neural circuits underlying adaptation and learning in the perception of auditory space
King, A. J., Dahmen, J. C., Keating, P., Leach, N. D., Nodal, F. R., & Bajo, V. M. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.008 · Cited by 46
Sarter, 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
“a: The rodent Sustained Attention Task (SAT) consists of a randomized sequence of cue and noncue events, followed by extension of the two response ports (McGaughy et al., 1996; McGaughy and Sarter, 1995; St Peters et al., 2011a).”
Self-citationMiner, L. A. H., Ostrander, M. M., & Sarter, M. F. (1997) · Journal of Psychopharmacology · doi:10.1177/026988119701100210 · Cited by 47
“For example, basal forebrain lesions spared the animals’ ability to reject non-signal events but decreased the hit rate well below 30 percent (McGaughy et al., 1996).”
BackgroundMethodResultInfluentialSelf-citationRoss, R. S., McGaughy, J. A., & Eichenbaum, H. (2005) · Learning & Memory · doi:10.1101/lm.91605 · Cited by 46
“Lesions of the NBM/SI have been shown to impair sustained (McGaughy et al. 1996) and divided attention (Turchi and Sarter 1997), but these lesions deplete the cholinergic innervation of the entire neocortical mantle.”
BackgroundSelf-citationDiminished 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 47
“SAT performance depends on the integrity of the cholinergic system (McGaughy et al., 1996) and is mediated via increases in cholinergic neurotransmission (Apparsundaram et al., 2005; St Peters et al., 2011).”
BackgroundSelf-citationPreferential cholinergic excitation of corticopontine neurons
Baker, A. L., O’Toole, R. J., & Gulledge, A. T. (2018) · The Journal of Physiology · doi:10.1113/jp275194 · Cited by 43
“For instance, loss of cholinergic input to the PFC impairs attention (Dalley et al., 2004; McGaughy et al., 2002; McGaughy et al., 1996; Newman and McGaughy, 2008), whereas enhancement of cholinergic signaling in rodents (Kolisnyk et al., 2013a), primates (Lange et al., 2015), and humans (Bentley…”
BackgroundBazalakova, M. H., & Blakely, R. (2006) · Handbook of experimental pharmacology · doi:10.1007/3-540-29784-7_21 · Cited by 44
“In a modern refinement of these studies, Apparsundaram and colleagues have examined CHT-mediated HACU in a behavioral paradigm that specifically taxes attentional effort and therefore depends on intact cortical cholinergic circuits ( McGaughy et al. 1996; Apparsundaram et al. 2005).”
Harati, H., Barbelivien, A., Cosquer, B., Majchrzak, M. J., & Cassel, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.031 · Cited by 43
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“These include covert orienting in primates (Voytko et al. 1994; Voytko 1996) and selective (Muir et al. 1994, 1995, 1996; Robbins et al. 1998), “incremental” (Chiba et al. 1995), divided (Turchi and Sarter 1997) and sustained (McGaughy et al. 1996) attention in rats.”
BackgroundRezvani, A. H., Kholdebarin, E., Dawson, E. A., & Levin, E. D. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145706007528 · Cited by 42
Selective lesions of the nucleus basalis magnocellularis impair cognitive flexibility.
Cabrera, S. M., Chavez, C. M., Corley, S. R., Kitto, M. R., & Butt, A. E. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.298 · Cited by 42
“Impairments in operant measures of sustained attention or vigilance (McGaughy, Decker, & Sarter, 1999; McGaughy, Kaiser, & Sarter, 1996; McGaughy & Sarter, 1998) and impairments in divided attention (Turchi & Sarter, 1997; Waite, Wardlow, & Power, 1999) have been reported following selective NBM lesions.”
BackgroundCholinergic 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 43
Rivastigmine is associated with restoration of left frontal brain activity in Parkinson's disease
Possin, K. L., Kang, G. A., Guo, C. C., Fine, E. M., Trujillo, A. J., Racine, C. A., Wilheim, R., Johnson, E. T., Witt, J. L., Seeley, W. W., et al. (2013) · Movement Disorders · doi:10.1002/mds.25575 · Cited by 41
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Self-citationSelective immunolesions of CH4 cholinergic neurons do not disrupt spatial memory in rats
Galani, R., Lehmann, O., Bolmont, T., Aloy, E. M., Bertrand, F., Lazarus, C., Jeltsch‐David, H., & Cassel, J. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00674-1 · Cited by 41
“In other experiments, despite or because of cholinergic denervation of the cortex, 192-IgG-saporin-induced lesions of NBM cholinergic neurons failed to alter taste aversion learning [25], impaired attentional processes [26], altered water-maze performances, but probably because of nonmnemonic effects [23].”
BackgroundAttention as a target of intoxication:
Bushnell, P. J., Levin, E. D., Marrocco, R. T., Sarter, M. F., Strupp, B. J., & Warburton, D. M. (2000) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(00)00077-5 · Cited by 40
Self-citationModeling Deficits in Attention, Inhibition, and Flexibility in HAND
Moran, L. M., Booze, R. M., & Mactutus, C. F. (2014) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-014-9539-z · Cited by 38
“…2004), and DA receptor activity regulates cortical ACh efflux (Moore et al. 1999; Zmarowski et al. 2005), which is essential in the mediation of attentional processes , as demonstrated with the signal detection task which taps sustained attention (McGaughy et al. 1996; Himmelheber et al. 2000).”
Sarter, M. F., Martínez, V., & Kozak, R. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1216-6 · Cited by 42
“Cholinergic lesions selectively disrupt the detection of signals in the task described above, sparing non-signal trial performance (McGaughy et al. 1996).”
BackgroundSelf-citationBroussard, J. I., Sarter, M. F., & Givens, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.030 · Cited by 40
“This task has previously demonstrated the necessity of the cholinergic input to the cortex in maintaining the detection of visual signals, whereas nonsignal performance remained unaffected (McGaughy et al., 1996; McGaughy and Sarter, 1999).”
BackgroundSelf-citationKozak, R., Bowman, E. M., Latimer, M. P., Rostron, C. L., & Winn, P. (2004) · Experimental Brain Research · doi:10.1007/s00221-004-2143-3 · Cited by 40
“To clarify the attentional nature of the task, we tested the sensitivity of PPTg deficits to changes in target signal duration, a procedure that has been used as a manipulation of attentional load (McGaughy et al. 1996).”
MethodSignal detection behavior in humans and rats: a comparison with matched tasks
Bushnell, P. J., Benignus, V. A., & Case, M. (2003) · Behavioural Processes · doi:10.1016/s0376-6357(03)00146-3 · Cited by 39
Neigh, G. N., Arnold, H. M., Rabenstein, R. L., Sarter, M. F., & Bruno, J. P. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.10.006 · Cited by 39
“Numerous studies have demonstrated that activity within the BFCS is necessary for performance in tasks designed to explicitly measure attention (Muir et al., 1992, 1994; McGaughy et al., 1996).”
Self-citationExtensive Lesions of Cholinergic Basal Forebrain Neurons Do Not Impair Spatial Working Memory
Vuckovich, J. A., Semel, M. E., & Baxter, M. G. (2004) · Learning & Memory · doi:10.1101/lm.63504 · Cited by 39
“Attentional defects are reliably observed after selective loss of basal forebrain cholinergic neurons (McGaughy et al. 1996; Sarter et al. 1997; McGaughy and Sarter 1998; Sarter and Bruno 1999).”
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
“Rationale—Initial attempts to train mice to SAT criterion performance (defined below), using retractable levers similar to the rat version of the task [1,12,42,43,56], failed to generate stable and useful levels of performance.”
BackgroundSelf-citationClark, S. D., Alderson, H. L., Winn, P., et al. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04529.x · Cited by 38
“In contrast, 192-saporin, introduced by Wiley et al. (1991), has successfully helped define the importance of basal forebrain cholinergic neurons in, for example, attention and learning (Torres et al. 1994; McGaughy et al. 1996, 2000; Chudasama et al. 2004).”
BackgroundMicrodialysis and its use in behavioural studies: Focus on acetylcholine.
König, M., Thinnes, A., & Klein, J. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.08.013 · Cited by 33
“Lesion experiments showed that these projections are necessary for performing tasks that require attention (McGaughy et al., 1996, 2002; Dalley et al., 2001).”
Lateralized Attentional Functions of Cortical Cholinergic Inputs.
Martínez, V., & Sarter, M. F. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.5.984 · Cited by 38
Self-citationNieto-Escámez, F. A., Sánchez-Santed, F., & de Bruin, J. P. C. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00458-2 · Cited by 37
Detection of visual signals by rats: effects of signal intensity, event rate, and task type
Bushnell, P. J. (1999) · Behavioural Processes · doi:10.1016/s0376-6357(99)00030-3 · Cited by 37
Roßner, S. (1997) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(97)00035-x · Cited by 36
Corticotropin releasing factor impairs sustained attention in male and female rats
Cole, R. D., Kawasumi, Y., Parikh, V., & Bangasser, D. A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.023 · Cited by 35
“The present study addressed this gap by determining whether central CRF disrupted sustained attention using a well-established sustained attention task (SAT) in which rats were trained to detect signaled from non-signaled trials [11, 12].”
BackgroundMethodResultWinters, B. D., & Dunnett, S. B. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.3.546 · Cited by 37
Fadel, J. R., Moore, H. M., Sarter, M. F., & Bruno, J. P. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06592.1996 · Cited by 35
“In this regard, we have reported enduring performance deficits in these 192 IgG-saporin-treated animals in operant tasks of sustained (McGaughy et al., 1996) and divided (Turchi et al., 1995) attention.”
Self-citationGastard, M. C., Jensen, S. L., Martin, J. R., Williams, E. A., & Zahm, D. S. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03513-8 · Cited by 35
Maddux, J.-M., & Holland, P. C. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.031 · Cited by 35
Montero-Pastor, A., Vale-Martı́nez, A., Guillazo‐Blanch, G., & Martí‐Nicolovius, M. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.01.017 · Cited by 33
Chronic nicotine interactions with clozapine and risperidone and attentional function in rats
Rezvani, A. H., Caldwell, D. P., & Levin, E. D. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.10.017 · Cited by 33
Berntson, G. G., Shafi, R., Knox, D., & Sarter, M. F. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00702-9 · Cited by 33
Self-citationBushnell, P. J., Chiba, A. A., & Oshiro, W. M. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00082-x · Cited by 31
Behavioural Vigilance in Schizophrenia
Mar, C. M., Smith, D. A. F., & Sarter, M. F. (1996) · The British Journal of Psychiatry · doi:10.1192/bjp.169.6.781 · Cited by 32
Self-citationLiu, R., Crawford, J., Callahan, P. M., Terry, A. V., Constantinidis, C., & Blake, D. T. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.026 · Cited by 31
Kucinski, A. J., Phillips, K. B., Cherian, A. K., & Sarter, M. F. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05354-5 · Cited by 29
Self-citationCell Assemblies of the Basal Forebrain
Tingley, D., Alexander, A. S., Quinn, L. K., Chiba, A. A., & Nitz, D. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4432-14.2015 · Cited by 34
“…learning, neural representation and responsiveness (Buzsáki et al., 1988; Wilson and Rolls, 1990a,b; Chiba et al., 1995; Bakin and Weinberger, 1996; McGaughy et al., 1996; Kilgard and Merzenich, 1998; Szymusiak et al., 2000; Conner et al., 2003; Lee et al., 2004; Holland and Gallagher, 2006;…”
BackgroundPaolone, G., Lee, T. M., & Sarter, M. F. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2271-12.2012 · Cited by 32
“…increases in cholinergic activity for maintaining diurnal activity patterns, we lesioned the cholinergic projections to cortical regions using the immunotoxin 192 IgG saporin (192-SAP; Advanced Targeting System) in animals that reached stable SAT performance (McGaughy et al., 1996, 2000).”
BackgroundMethodSelf-citationDürschmid, S., Reichert, C., Kuhn, J., Freund, H., Hinrichs, H., & Heinze, H. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.13749 · Cited by 31
“…the enhancement of cortical plasticity (Rasmusson, 2000) and is involved in many cognitive functions including attention (Voytko et al., 1994; McGaughy et al.,1996; Sarter & Bruno, 2000; Furey et al., 2008; Herrero et al., 2008) and memory encoding/learning (Miasnikov et al., 2001, 2008;…”
BackgroundPerformance of galanin transgenic mice in the 5-choice serial reaction time attentional task
Wrenn, C. C., Turchi, J. N., Schlosser, S., Dreiling, J. L., Stephenson, D., & Crawley, J. N. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.03.003 · Cited by 31
Dillon, G. M., Shelton, D. S., McKinney, A. P., Caniga, M., Marcus, J., Ferguson, M. T., Kornecook, T. J., & Dodart, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.036 · Cited by 30
Tian, M. K., Bailey, C. D. C., Biasi, M. D., Picciotto, M. R., & Lambe, E. K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3600-11.2011 · Cited by 29
“The loss of prefrontal ACh afferents, by contrast, substantially lowers cue detection in attention tasks (McGaughy et al., 1996).”
BackgroundMartínez, V., Parikh, V., & Sarter, M. F. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.02.005 · Cited by 30
Self-citation
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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