How to Cite
Venegas, J. P., Navarrete, M., Orellana-Garcia, L., Rojas, M., Avello-Duarte, F., & Nunez-Parra, A. (2023). Basal forebrain modulation of olfactory coding in vivo. International Journal of Psychological Research, 16(2), 62–86. https://doi.org/10.21500/20112084.6486
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Sensory perception is one of the most fundamental brain functions allowing individuals to properly interact and adapt to a constantly changing environment. This process requires the integration of bottom-up and top-down neuronal activity that is centrally mediated by the basal forebrain, a brain region that has been linked to a series of cognitive processes such as attention and alertness.

Here, we review the latest research using optogenetic approaches in rodents and in vivo electrophysiological recordings that are shedding light into the role of this region regulating olfactory processing and decision-making. Moreover, we summarize evidence highlighting the anatomical and physiological differences in the basal forebrain of individuals with autism spectrum disorder, which could underpin the sensory perception abnormalities they exhibit and propose this research line as a potential opportunity to understand the neurobiological basis of this disorder.



Agostinelli, L. J., Geerling, J. C., & Scammell, T. E. (2019). Basal forebrain subcortical projections. Brain Structure and Function, 224(3), 1097–1117. https://doi.org/10.1007/s00429-018-01820-6
Alitto, H. J., & Dan, Y. (2012). Cell-type-specific modulation of neocortical activity by basal forebrain input. Frontiers in Systems Neuroscience, 6(DEC), 1–12. https://doi.org/10.3389/fnsys.2012.00079
Alonso, M., Lepousez, G., Wagner, S., Bardy, C., Gabellec, M. M., Torquet, N., & Lledo, P. M. (2012). Activation of adult-born neurons facilitates learning and memory. Nature Neuroscience, 15(6), 897–904. https://doi.org/10.1038/nn.3108
Alonso, M., Viollet, C., Gabellec, M. M., Meas-Yedid, V., Olivo-Marin, J. C., & Lledo, P. M. (2006). Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. Journal of Neuroscience, 26(41), 10508–10513. https://doi.org/10.1523/JNEUROSCI.2633-06.2006
Altman, J., & Das, G. D. (1965). Post-Natal Origin of Microneurones in the Rat Brain. Nature, 207(5000), 953–956. https://doi.org/10.1038/207953a0
American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders (DSM-5-TR) (American Psychiatric Publishing (ed.); Fifth Edit). https://doi.org/https://doi.org/10.1176/appi.books.9780890425596
Apicella, A., Yuan, Q., Scanziani, M., & Isaacson, J. S. (2010). Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. Journal of Neuroscience, 30(42), 14255–14260. https://doi.org/10.1523/JNEUROSCI.2747-10.2010
Arruda, D., Publio, R., & Roque, A. C. (2013). The Periglomerular Cell of the Olfactory Bulb and its Role in Controlling Mitral Cell Spiking: A Computational Model. PLoS ONE, 8(2), e56148. https://doi.org/10.1371/journal.pone.0056148
Ashwin, C., Chapman, E., Howells, J., Rhydderch, D., Walker, I., & Baron-Cohen, S. (2014). Enhanced olfactory sensitivity in autism spectrum conditions. Molecular Autism, 5(1), 1–9. https://doi.org/10.1186/2040-2392-5-53
Bacchelli, E., Battaglia, A., Cameli, C., Lomartire, S., Tancredi, R., Thomson, S., Sutcliffe, J. S., & Maestrini, E. (2015). Analysis of CHRNA7 rare variants in autism spectrum disorder susceptibility. American Journal of Medical Genetics, Part A, 167(4), 715–723. https://doi.org/10.1002/ajmg.a.36847
Bangerter, A., Ness, S., Aman, M. G., Esbensen, A. J., Goodwin, M. S., Dawson, G., Hendren, R., Leventhal, B., Khan, A., Opler, M., Harris, A., & Pandina, G. (2017). Autism Behavior Inventory: A Novel Tool for Assessing Core and Associated Symptoms of Autism Spectrum Disorder. Journal of Child and Adolescent Psychopharmacology, 27(9), 814–822. https://doi.org/10.1089/cap.2017.0018
Bastiaansen, M. C. M., & Brunia, C. H. M. (2001). Anticipatory attention: An event-related desynchronization approach. International Journal of Psychophysiology, 43(1), 91–107. https://doi.org/10.1016/S0167-8760(01)00181-7
Bauman, M., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35(6), 866–874. https://doi.org/10.1212/wnl.35.6.866
Bendahmane, M., Ogg, M. C., Ennis, M., & Fletcher, M. L. (2016). Increased olfactory bulb acetylcholine bi-directionally modulates glomerular odor sensitivity. Scientific Reports, 6(April), 1–13. https://doi.org/10.1038/srep25808
Bennetto, L., Kuschner, E. S., & Hyman, S. L. (2007). Olfaction and Taste Processing in Autism. Biological Psychiatry, 62(9), 1015–1021. https://doi.org/10.1016/j.biopsych.2007.04.019
Bodaleo, F., Tapia-Monsalves, C., Cea-Del Rio, C., Gonzalez-Billault, C., & Nunez-Parra, A. (2019). Structural and functional abnormalities in the olfactory system of fragile x syndrome models. In Frontiers in Molecular Neuroscience (Vol. 12). Frontiers Media S.A. https://doi.org/10.3389/fnmol.2019.00135
Böhm, E., Brunert, D., & Rothermel, M. (2020). Input dependent modulation of olfactory bulb activity by HDB GABAergic projections. Scientific Reports, 10(1), 1–15. https://doi.org/10.1038/s41598-020-67276-z
Boudjarane, M. A., Grandgeorge, M., Marianowski, R., Misery, L., & Lemonnier, É. (2017). Perception of odors and tastes in autism spectrum disorders: A systematic review of assessments. Autism Research, 10(6), 1045–1057. https://doi.org/10.1002/aur.1760
Bouret, S., & Sara, S. J. (2004). Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. European Journal of Neuroscience, 20(3), 791–802. https://doi.org/10.1111/j.1460-9568.2004.03526.x
Bowles, S., Hickman, J., Peng, X., Williamson, W. R., Huang, R., Washington, K., Donegan, D., & Welle, C. G. (2022). Vagus nerve stimulation drives selective circuit modulation through cholinergic reinforcement. Neuron, 110(17), 2867-2885.e7. https://doi.org/10.1016/j.neuron.2022.06.017
Boyd, A. M., Sturgill, J. F., Poo, C., & Isaacson, J. S. (2012). Cortical Feedback Control of Olfactory Bulb Circuits. Neuron, 76(6), 1161–1174. https://doi.org/10.1016/j.neuron.2012.10.020
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neuroscience, 8(9), 1263–1268. https://doi.org/10.1038/nn1525
Broadbent, D. E. (1958). Perception and communication. In Perception and communication. Pergamon Press. https://doi.org/10.1037/10037-000
Bronshteín, A. A., & Minor, A. V. (1977). [Regeneration of olfactory flagella and restoration of the electroolfactogram following application of triton X-100 to the olfactory mucosa of frogs]. Tsitologiia, 19(1), 33–39.
Brunert, D., & Rothermel, M. (2019). Neuromodulation of early sensory processing in the olfactory system. Neuroforum, 25(1), 25–38. https://doi.org/10.1515/nf-2018-0021
Buck, L. B. (1992). A novel multigene family may encode odorant receptors. Society of General Physiologists Series, 65(1), 175–187. https://doi.org/10.1016/0092-8674(91)90418-x
Burton, S. D. (2017). Inhibitory circuits of the mammalian main olfactory bulb. Journal of Neurophysiology, 118(4), 2034–2051. https://doi.org/10.1152/jn.00109.2017
Burton, S. D., LaRocca, G., Liu, A., Cheetham, C. E. J., & Urban, N. N. (2017). Olfactory bulb deep short-axon cells mediate widespread inhibition of tufted cell apical dendrites. Journal of Neuroscience, 37(5), 1117–1138. https://doi.org/10.1523/JNEUROSCI.2880-16.2016
Buzsaki, G., Bickford, R. G., Ponomareff, G., Thal, L. J., Mandel, R., & Gage, F. H. (1988). Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. Journal of Neuroscience, 8(11), 4007–4026. https://doi.org/10.1523/jneurosci.08-11-04007.1988
Cang, J., & Isaacson, J. S. (2003). In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. Journal of Neuroscience, 23(10), 4108–4116. https://doi.org/10.1523/jneurosci.23-10-04108.2003
Cascio, C. J., Gu, C., Schauder, K. B., Key, A. P., & Yoder, P. (2015). Somatosensory Event-Related Potentials and Association with Tactile Behavioral Responsiveness Patterns in Children with ASD. Brain Topography, 28(6), 895–903. https://doi.org/10.1007/s10548-015-0439-1
Case, D. T., Burton, S. D., Gedeon, J. Y., Williams, S. P. G., Urban, N. N., & Seal, R. P. (2017). Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nature Communications, 8(1), 652. https://doi.org/10.1038/s41467-017-00765-4
Castillo, P. E., Carleton, A., Vincent, J. D., & Lledo, P. M. (1999). Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. Journal of Neuroscience, 19(21), 9180–9191. https://doi.org/10.1523/jneurosci.19-21-09180.1999
Caulfield, M. P. (1993). Muscarinic Receptors—Characterization, coupling and function. Pharmacology & Therapeutics, 58(3), 319–379. https://doi.org/https://doi.org/10.1016/0163-7258(93)90027-B
Chaves-Coira, I., Martín-Cortecero, J., Nuñez, A., & Rodrigo-Angulo, M. L. (2018a). Basal Forebrain Nuclei Display Distinct Projecting Pathways and Functional Circuits to Sensory Primary and Prefrontal Cortices in the Rat. Frontiers in Neuroanatomy, 12(August), 1–15. https://doi.org/10.3389/fnana.2018.00069
Chaves-Coira, I., Rodrigo-Angulo, M. L., & Nuñez, A. (2018b). Bilateral Pathways from the Basal Forebrain to Sensory Cortices May Contribute to Synchronous Sensory Processing. Frontiers in Neuroanatomy, 12, 5. https://doi.org/10.3389/fnana.2018.00005
Chen, Y., Chen, X., Baserdem, B., Zhan, H., Li, Y., Davis, M. B., Kebschull, J. M., Zador, A. M., Koulakov, A. A., & Albeanu, D. F. (2022). High-throughput sequencing of single neuron projections reveals spatial organization in the olfactory cortex. Cell, 185(22), 4117-4134.e28. https://doi.org/10.1016/j.cell.2022.09.038
Chez, M. G., Aimonovitch, M., Buchanan, T., Mrazek, S., & Tremb, R. J. (2004). Treating autistic spectrum disorders in children: utility of the cholinesterase inhibitor rivastigmine tartrate. Journal of Child Neurology, 19(3), 165–169.
Chien, Y. L., Gau, S. S. F., Shang, C. Y., Chiu, Y. N., Tsai, W. C., & Wu, Y. Y. (2015). Visual memory and sustained attention impairment in youths with autism spectrum disorders. Psychological Medicine, 45(11), 2263–2273. https://doi.org/10.1017/S0033291714003201
Chilian, B., Abdollahpour, H., Bierhals, T., Haltrich, I., Fekete, G., Nagel, I., Rosenberger, G., & Kutsche, K. (2013). Dysfunction of SHANK2 and CHRNA7 in a patient with intellectual disability and language impairment supports genetic epistasis of the two loci. Clinical Genetics, 84(6), 560–565. https://doi.org/10.1111/cge.12105
Chong, E., Moroni, M., Wilson, C., Shoham, S., Panzeri, S., & Rinberg, D. (2020). Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception. Science, 368(6497). https://doi.org/10.1126/science.aba2357
Chung, S., & Son, J. W. (2020). Visual perception in autism spectrum disorder: A review of neuroimaging studies. Journal of the Korean Academy of Child and Adolescent Psychiatry, 31(3), 105–120. https://doi.org/10.5765/jkacap.200018
Constanti, A., & Sim, J. A. (1987). Muscarinic receptors mediating suppression of the M-current in guinea-pig olfactory cortex neurones may be of the M2-subtype. British Journal of Pharmacology, 90(1), 3–5. https://doi.org/10.1111/j.1476-5381.1987.tb16818.x
D’Souza, R. D., & Vijayaraghavan, S. (2012). Nicotinic Receptor-Mediated Filtering of Mitral Cell Responses to Olfactory Nerve Inputs Involves the α3β4 Subtype. The Journal of Neuroscience, 32(9), 3261 LP – 3266. https://doi.org/10.1523/JNEUROSCI.5024-11.2012
D’Souza, R. D., & Vijayaraghavan, S. (2014). Paying attention to smell: Cholinergic signaling in the olfactory bulb. Frontiers in Synaptic Neuroscience, 6(SEP), 1–11. https://doi.org/10.3389/fnsyn.2014.00021
de Almeida, L., Idiart, M., & Linster, C. (2013). A model of cholinergic modulation in olfactory bulb and piriform cortex. Journal of Neurophysiology, 109(5), 1360–1377. https://doi.org/10.1152/jn.00577.2012
De Rosa, E., & Hasselmo, M. E. (2000). Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behavioral Neuroscience, 114(1), 32–41. https://doi.org/10.1037/0735-7044.114.1.32
De Rosa, E., Hasselmo, M. E., & Baxtera, M. G. (2001). Contribution of the cholinergic basal forebrain to proactive interference from stored odor memories during associative learning in rats. Behavioral Neuroscience, 115(2), 314–327. https://doi.org/10.1037/0735-7044.115.2.314
Devore, S., de Almeida, L., & Linster, C. (2014). Distinct roles of bulbar muscarinic and nicotinic receptors in olfactory discrimination learning. Journal of Neuroscience, 34(34), 11244–11260. https://doi.org/10.1523/JNEUROSCI.1499-14.2014
Devore, S., & Linster, C. (2012). Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Frontiers in Behavioral Neuroscience, 6, 52. https://doi.org/10.3389/fnbeh.2012.00052
Devore, S., Pender-Morris, N., Dean, O., Smith, D., & Linster, C. (2016). Basal forebrain dynamics during nonassociative and associative olfactory learning. Journal of Neurophysiology, 115(1), 423–433. https://doi.org/10.1152/jn.00572.2015
Do, J. P., Xu, M., Lee, S. H., Chang, W. C., Zhang, S., Chung, S., Yung, T. J., Fan, J. L., Miyamichi, K., Luo, L., & Dan, Y. (2016). Cell type-specific long-range connections of basal forebrain circuit. ELife, 5(September), 1–18. https://doi.org/10.7554/eLife.13214
Doty, R. L. (1986). Odour-guided behaviour in mammals. Experientia, 42(3), 257–271. https://doi.org/10.1007/BF01942506
Doucette, W., Gire, D. H., Whitesell, J., Carmean, V., Lucero, M. T., & Restrepo, D. (2011). Associative cortex features in the first olfactory brain relay station. Neuron, 69(6), 1176–1187. https://doi.org/10.1016/j.neuron.2011.02.024
Doucette, W., & Restrepo, D. (2008). Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biology, 6(10), 2266–2285. https://doi.org/10.1371/journal.pbio.0060258
Dudova, I., Vodicka, J., Havlovicova, M., Sedlacek, Z., Urbanek, T., & Hrdlicka, M. (2011). Odor detection threshold, but not odor identification, is impaired in children with autism. European Child and Adolescent Psychiatry, 20(7), 333–340. https://doi.org/10.1007/s00787-011-0177-1
Ergaz, Z., Weinstein-Fudim, L., & Ornoy, A. (2016). Genetic and non-genetic animal models for autism spectrum disorders (ASD). Reproductive Toxicology, 64, 116–140. https://doi.org/10.1016/j.reprotox.2016.04.024
Eyre, M. D., Antal, M., & Nusser, Z. (2008). Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar gabaergic connections. Journal of Neuroscience, 28(33), 8217–8229. https://doi.org/10.1523/JNEUROSCI.2490-08.2008
Fletcher, M. L., & Chen, W. R. (2010). Neural correlates of olfactory learning: Critical role of centrifugal neuromodulation. Learning and Memory, 17(11), 561–570. https://doi.org/10.1101/lm.941510
Foss-Feig, J. H., Heacock, J. L., & Cascio, C. J. (2012). Tactile responsiveness patterns and their association with core features in autism spectrum disorders. Research in Autism Spectrum Disorders, 6(1), 337–344. https://doi.org/10.1016/j.rasd.2011.06.007
Friedman, S. D., Shaw, D. W. W., Artru, A. A., Dawson, G., Petropoulos, H., & Dager, S. R. (2006). Gray and white matter brain chemistry in young children with autism. Archives of General Psychiatry, 63(7), 786–794. https://doi.org/10.1001/archpsyc.63.7.786
Friedman, Shaw, D. W., Artru, A. A., Richards, T. L., Gardner, J., Dawson, G., Posse, S., & Dager, S. R. (2003). Regional brain chemical alterations in young children with autism spectrum disorder. Neurology, 60(1), 100–107. https://doi.org/10.1212/WNL.60.1.100
Friedrich, R. W., & Korsching, S. I. (1997). Combinatorial and Chemotopic Odorant Coding in the Zebrafish Olfactory Bulb Visualized by Optical Imaging. Neuron, 18(5), 737–752. https://doi.org/10.1016/S0896-6273(00)80314-1
Fukunaga, I., Herb, J. T., Kollo, M., Boyden, E. S., & Schaefer, A. T. (2014). Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb. Nature Neuroscience, 17(9), 1208–1216. https://doi.org/10.1038/nn.3760
Gadziola, M. A., Stetzik, L. A., Wright, K. N., Milton, A. J., Arakawa, K., del Mar Cortijo, M., & Wesson, D. W. (2020). A Neural System that Represents the Association of Odors with Rewarded Outcomes and Promotes Behavioral Engagement. Cell Reports, 32(3). https://doi.org/10.1016/j.celrep.2020.107919
Ghaleiha, A., Ghyasvand, M., Mohammadi, M. R., Farokhnia, M., Yadegari, N., Tabrizi, M., Hajiaghaee, R., Yekehtaz, H., & Akhondzadeh, S. (2014). Galantamine efficacy and tolerability as an augmentative therapy in autistic children: A randomized, double-blind, placebo-controlled trial. Journal of Psychopharmacology, 28(7), 677–685. https://doi.org/10.1177/0269881113508830
Gheusi, G., Lepousez, G., & Lledo, P. (2013). Adult-Born Neurons in the Olfactory Bulb : Integration and Functional Consequences. Current Topics in Behavioral Neurosciences, 15, 49–72. https://doi.org/10.1007/7854
Ghosh, S., Larson, S. D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., & Baldwin, K. K. (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature, 472(7342), 217–222. https://doi.org/10.1038/nature09945
Gielow, M. R., & Zaborszky, L. (2017). The Input-Output Relationship of the Cholinergic Basal Forebrain. Cell Reports, 18(7), 1817–1830. https://doi.org/10.1016/j.celrep.2017.01.060
Gill, J. V., Lerman, G. M., Zhao, H., Stetler, B. J., Rinberg, D., & Shoham, S. (2020). Precise Holographic Manipulation of Olfactory Circuits Reveals Coding Features Determining Perceptual Detection. Neuron, 108(2), 382-393.e5. https://doi.org/10.1016/j.neuron.2020.07.034
Gire, D. H., & Schoppa, N. E. (2009). Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. Journal of Neuroscience, 29(43), 13454–13464. https://doi.org/10.1523/JNEUROSCI.2368-09.2009
Gire, D. H., Whitesell, J. D., Doucette, W., & Restrepo, D. (2013). Information for decision-making and stimulus identification is multiplexed in sensory cortex. Nature Neuroscience, 16(8), 991–993. https://doi.org/10.1038/nn.3432
Goard, M., & Dan, Y. (2009). Basal forebrain activation enhances cortical coding of natural scenes. Nature Neuroscience, 12(11), 1444–1449. https://doi.org/10.1038/nn.2402
Gracia-Llanes, F. J., Crespo, C., Blasco-Ibáñez, J. M., Nacher, J., Varea, E., Rovira-Esteban, L., & Martínez-Guijarro, F. J. (2010). GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb. Neuroscience, 170(3), 913–922. https://doi.org/10.1016/j.neuroscience.2010.07.046
Gritti, I., Henny, P., Galloni, F., Mainville, L., Mariotti, M., & Jones, B. E. (2006). Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience, 143(4), 1051–1064. https://doi.org/10.1016/j.neuroscience.2006.09.024
Gritti, I., Mainville, L., Mancia, M., & Jones, B. E. (1997). GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. Journal of Comparative Neurology, 383(2), 163–177. https://doi.org/10.1002/(SICI)1096-9861(19970630)383:2<163::AID-CNE4>3.0.CO;2-Z
Grossberg, S., Palma, J., & Versace, M. (2016). Resonant cholinergic dynamics in cognitive and motor decision-making: Attention, category learning, and choice in neocortex, superior colliculus, and optic tectum. Frontiers in Neuroscience, 9(JAN), 1–26. https://doi.org/10.3389/fnins.2015.00501
Gschwend, O., Beroud, J., & Carleton, A. (2012). Encoding odorant identity by spiking packets of Rate-Invariant neurons in awake mice. PLoS ONE, 7(1), e30155. https://doi.org/10.1371/journal.pone.0030155
Guo, W., Robert, B., & Polley, D. B. (2019). The Cholinergic Basal Forebrain Links Auditory Stimuli with Delayed Reinforcement to Support Learning. Neuron, 103(6), 1164-1177.e6. https://doi.org/10.1016/j.neuron.2019.06.024
Gupta, R., Koscik, T. R., Bechara, A., & Tranel, D. (2011). The amygdala and decision-making. Neuropsychologia, 49(4), 760–766. https://doi.org/10.1016/j.neuropsychologia.2010.09.029
Han, Y., Shi, Y. F., Xi, W., Zhou, R., Tan, Z. B., Wang, H., Li, X. M., Chen, Z., Feng, G., Luo, M., Huang, Z. L., Duan, S., & Yu, Y. Q. (2014). Selective activation of cholinergic basal forebrain neurons induces immediate sleep-wake transitions. Current Biology, 24(6), 693–698. https://doi.org/10.1016/j.cub.2014.02.011
Hangya, B., Ranade, S. P., Lorenc, M., & Kepecs, A. (2015). Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback. Cell, 162(5), 1155–1168. https://doi.org/10.1016/j.cell.2015.07.057
Hanson, E., Brandel-Ankrapp, K. L., & Arenkiel, B. R. (2021). Dynamic Cholinergic Tone in the Basal Forebrain Reflects Reward-Seeking and Reinforcement During Olfactory Behavior. Frontiers in Cellular Neuroscience, 15(February), 1–14. https://doi.org/10.3389/fncel.2021.635837
Hanson, E., Swanson, J., & Arenkiel, B. R. (2020). GABAergic Input From the Basal Forebrain Promotes the Survival of Adult-Born Neurons in the Mouse Olfactory Bulb. Frontiers in Neural Circuits, 14(April), 1–12. https://doi.org/10.3389/fncir.2020.00017
Hardan, A. Y., & Handen, B. L. (2002). A retrospective open trial of adjunctive donepezil in children and adolescents with autistic disorder. Journal of Child and Adolescent Psychopharmacology, 12(3), 237–241. https://doi.org/10.1089/104454602760386923
Hasselmo, M. E., & Bower, J. M. (1992). Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. Journal of Neurophysiology, 67(5), 1222–1229. https://doi.org/10.1152/jn.1992.67.5.1222
Hasselmo, Michael E., & Barkai, E. (1995). Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. Journal of Neuroscience, 15(10), 6592–6604. https://doi.org/10.1523/jneurosci.15-10-06592.1995
Hasselmo, Michael E., & Sarter, M. (2011). Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology, 36(1), 52–73. https://doi.org/10.1038/npp.2010.104
Hernández-Peón, R., Scherrer, H., & Jouvet, M. (1956). Modification of electric activity in cochlear nucleus during “attention” in unanesthetized cats. Science, 123(3191), 331–332. https://doi.org/10.1126/science.123.3191.331
Hodges, H., Fealko, C., & Soares, N. (2020). Autism spectrum disorder: Definition, epidemiology, causes, and clinical evaluation. Translational Pediatrics, 9(S1), S55–S65. https://doi.org/10.21037/tp.2019.09.09
Hoover, K. C. (2010). Smell with inspiration: The evolutionary significance of olfaction. American Journal of Physical Anthropology, 143(SUPPL. 51), 63–74. https://doi.org/10.1002/ajpa.21441
Hur, E. E., & Zaborszky, L. (2005). Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: A combined retrograde tracing in situ hybridization. Journal of Comparative Neurology, 483(3), 351–373. https://doi.org/10.1002/cne.20444
Igarashi, K. M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W. R., & Mori, K. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. Journal of Neuroscience, 32(23), 7970–7985. https://doi.org/10.1523/JNEUROSCI.0154-12.2012
Isaacson, J. S., & Strowbridge, B. W. (1998). Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS Electron microscopic evidence indicates that mitral cell dendrites contain synaptic vesicles clustered around active zones (Rall et al. Neuron, 20(4), 749–761.
Jahr, B. Y. C. E., & Nicoll, R. A. (1982). An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb. The Journal of Physiology, 326, 213–234. https://doi.org/10.1113/jphysiol.1982.sp014187
Jaramillo, S., & Zador, A. M. (2011). The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nature Neuroscience, 14(2), 246–253. https://doi.org/10.1038/nn.2688
Johnson, B., & Leon, M. (2007). Chemotopic Odorant Coding in a Mammalian Olfactory System. Journal of Comparative Neurology, 503(1), 1–34. https://doi.org/10.1002/cne.21396
Karvat, G., & Kimchi, T. (2014). Acetylcholine elevation relieves cognitive rigidity and social deficiency in a mouse model of autism. Neuropsychopharmacology, 39(4), 831–840. https://doi.org/10.1038/npp.2013.274
Kay, L. M. (2005). Theta oscillations and sensorimotor performance. Proceedings of the National Academy of Sciences of the United States of America, 102(10), 3863–3868. https://doi.org/10.1073/pnas.0407920102
Kemper, T., & Bauman, M. (1998). Neuropathology of Infantile Austism. Journal of Neuropathology and Experimenta Neurology, 57(7), 645–652. https://doi.org/10.1097/00005072-199807000-00001
Khalighinejad, N., Priestley, L., Jbabdi, S., & Rushworth, M. F. S. (2020). Human decisions about when to act originate within a basal forebrain-nigral circuit. Proceedings of the National Academy of Sciences of the United States of America, 117(21), 11799–11810. https://doi.org/10.1073/pnas.1921211117
Klinkenberg, I., Sambeth, A., & Blokland, A. (2011). Acetylcholine and attention. Behavioural Brain Research, 221(2), 430–442. https://doi.org/10.1016/j.bbr.2010.11.033
Koehler, L., Fournel, A., Albertowski, K., Roessner, V., Gerber, J., Hummel, C., Hummel, T., & Bensafi, M. (2018). Impaired odor perception in autism spectrum disorder is associated with decreased activity in olfactory cortex. Chemical Senses, 43(8), 627–634. https://doi.org/10.1093/chemse/bjy051
Koevoet, D., Deschamps, P. K. H., & Kenemans, J. L. (2021). Catecholaminergic and Cholinergic Neuromodulation in Autism Spectrum Disorder : A Comparison to Attention-Deficit Hyperactivity Disorder. PsyArXiv. https://doi.org/10.31234/osf.io/nb5j8
Kondo, H., & Zaborszky, L. (2016). Topographic organization of the basal forebrain projections to the perirhinal, postrhinal, and entorhinal cortex in rats. Journal of Comparative Neurology, 524(12), 2503–2515. https://doi.org/https://doi.org/10.1002/cne.23967
Kudryavitskaya, E., Marom, E., Shani-Narkiss, H., Pash, D., & Mizrahi, A. (2021). Flexible categorization in the mouse olfactory bulb. Current Biology, 31(8), 1616-1631.e4. https://doi.org/10.1016/j.cub.2021.01.063
Lagier, S., Carleton, A., & Lledo, P. M. (2004). Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb. Journal of Neuroscience, 24(18), 4382–4392. https://doi.org/10.1523/JNEUROSCI.5570-03.2004
Lam, K. S. L., Bodfish, J. W., & Piven, J. (2008). Evidence for three subtypes of repetitive behavior in autism that differ in familiality and association with other symptoms. Journal of Child Psychology and Psychiatry and Allied Disciplines, 49(11), 1193–1200. https://doi.org/10.1111/j.1469-7610.2008.01944.x
Laszlovszky, T., Schlingloff, D., Hegedüs, P., Freund, T. F., Gulyás, A., Kepecs, A., & Hangya, B. (2020). Distinct synchronization, cortical coupling and behavioral function of two basal forebrain cholinergic neuron types. Nature Neuroscience, 23(8), 992–1003. https://doi.org/10.1038/s41593-020-0648-0
Leach, N. D., Nodal, F. R., Cordery, P. M., King, A. J., & Bajo, V. M. (2013). Cortical cholinergic input is required for normal auditory perception and experience-dependent plasticity in adult ferrets. Journal of Neuroscience, 33(15), 6659–6671. https://doi.org/10.1523/JNEUROSCI.5039-12.2013
Lee, S. H., & Dan, Y. (2012). Neuromodulation of Brain States. Neuron, 76(1), 209–222. https://doi.org/10.1016/j.neuron.2012.09.012
Lewis, A. S., van Schalkwyk, G. I., Lopez, M. O., Volkmar, F. R., Picciotto, M. R., & Sukhodolsky, D. G. (2018). An Exploratory Trial of Transdermal Nicotine for Aggression and Irritability in Adults with Autism Spectrum Disorder. Journal of Autism and Developmental Disorders, 48(8), 2748–2757. https://doi.org/10.1007/s10803-018-3536-7
Li, G., & Cleland, T. (2013). A two-layer biophysical model of cholinergic neuromodulation in olfactory bulb. Journal of Neuroscience, 33(7), 3037–3058. https://doi.org/10.1523/JNEUROSCI.2831-12.2013
Li, X., Yu, B., Sun, Q., Zhang, Y., Ren, M., Zhang, X., Li, A., Yuan, J., Madisen, L., Luo, Q., Zeng, H., Gong, H., & Qiu, Z. (2018). Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons. Proceedings of the National Academy of Sciences of the United States of America, 115(2), 415–420. https://doi.org/10.1073/pnas.1703601115
Lim, D., & Alvarez-Buylla, A. (2016). The Adult Ventricular – Subventricular Zone and Olfactory bulb Neurogenesis. Cold Spring Harbor Perspectives in Biology, 8(5), a018820. https://www.ncbi.nlm.nih.gov/pubmed/27048191
Lin, S. C., Brown, R. E., Shuler, M. G. H., Petersen, C. C. H., & Kepecs, A. (2015). Optogenetic dissection of the basal forebrain neuromodulatory control of cortical activation, plasticity, and cognition. Journal of Neuroscience, 35(41), 13896–13903. https://doi.org/10.1523/JNEUROSCI.2590-15.2015
Lin, S. C., & Nicolelis, M. A. L. (2008). Neuronal Ensemble Bursting in the Basal Forebrain Encodes Salience Irrespective of Valence. Neuron, 59(1), 138–149. https://doi.org/10.1016/j.neuron.2008.04.031
Linster, C., Wyble, B. P., & Hasselmo, M. E. (1999). Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. Journal of Neurophysiology, 81(6), 2737–2742. https://doi.org/10.1152/jn.1999.81.6.2737
Liu, S., Shao, Z., Puche, A., Wachowiak, M., Rothermel, M., & Shipley, M. T. (2015). Muscarinic receptors modulate dendrodendritic inhibitory synapses to sculpt glomerular output. Journal of Neuroscience, 35(14), 5680–5692. https://doi.org/10.1523/JNEUROSCI.4953-14.2015
Lledo, P. M., & Valley, M. (2016). Adult olfactory bulb neurogenesis. Cold Spring Harbor Perspectives in Biology, 8(8). https://doi.org/10.1101/cshperspect.a018945
Lois, C., & Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proceedings of the National Academy of Sciences of the United States of America, 90(5), 2074–2077. https://doi.org/10.1073/pnas.90.5.2074
Lois, C., & Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science (New York, N.Y.), 264(5162), 1145–1148. https://doi.org/10.1126/science.8178174
Lowther, C., Costain, G., Stavropoulos, D. J., Melvin, R., Silversides, C. K., Andrade, D. M., So, J., Faghfoury, H., Lionel, A. C., Marshall, C. R., Scherer, S. W., & Bassett, A. S. (2015). Delineating the 15q13.3 microdeletion phenotype: A case series and comprehensive review of the literature. Genetics in Medicine, 17(2), 149–157. https://doi.org/10.1038/gim.2014.83
Luchicchi, A., Bloem, B., Viaña, J. N. M., Mansvelder, H. D., & Role, L. W. (2014). Illuminating the role of cholinergic signaling in circuits of attention and emotionally salient behaviors. Frontiers in Synaptic Neuroscience, 6(OCT), 1–10. https://doi.org/10.3389/fnsyn.2014.00024
Luskin, M. B., & Price, J. L. (1982). The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling techniques. Journal of Comparative Neurology, 209(3), 249–263. https://doi.org/10.1002/cne.902090304
Lyons-Warren, A. M., Herman, I., Hunt, P. J., & Arenkiel, B. (2021). A systematic-review of olfactory deficits in neurodevelopmental disorders: From mouse to human. Neuroscience and Biobehavioral Reviews, 125(January), 110–121. https://doi.org/10.1016/j.neubiorev.2021.02.024
Ma, M., & Luo, M. (2012). Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. Journal of Neuroscience, 32(30), 10105–10116. https://doi.org/10.1523/JNEUROSCI.0058-12.2012
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999). Combinatorial receptor codes for odors. Cell, 96(5), 713–723. https://doi.org/10.1016/S0092-8674(00)80581-4
Malun, D., & Brunjes, P. C. (1996). Development of olfactory glomeruli: Temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. Journal of Comparative Neurology, 368(1), 1–16. https://doi.org/10.1002/(SICI)1096-9861(19960422)368:1<1::AID-CNE1>3.0.CO;2-7
Mandairon, N., Sacquet, J., Garcia, S., Ravel, N., Jourdan, F., & Didier, A. (2006). Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. European Journal of Neuroscience, 24(12), 3578–3588. https://doi.org/10.1111/j.1460-9568.2006.05235.x
Manns, I. D., Mainville, L., & Jones, B. E. (2001). Evidence for glutamate, in addition to acetylcholine and GABA, neurotransmitter synthesis in basal forebrain neurons projecting to the entorhinal cortex. Neuroscience, 107(2), 249–263. https://doi.org/https://doi.org/10.1016/S0306-4522(01)00302-5
Mark, G. P., Shabani, S., Dobbs, L. K., & Hansen, S. T. (2011). Cholinergic modulation of mesolimbic dopamine function and reward. Physiology and Behavior, 104(1), 76–81. https://doi.org/10.1016/j.physbeh.2011.04.052
Martin-Ruiz, C. M., Lee, M., Perry, R. H., Baumann, M., Court, J. A., & Perry, E. K. (2004). Molecular analysis of nicotinic receptor expression in autism. Molecular Brain Research, 123(1), 81–90. https://doi.org/10.1016/j.molbrainres.2004.01.003
Matsutani, S. (2010). Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience, 169(1), 436–448. https://doi.org/10.1016/j.neuroscience.2010.05.001
Matsutani, S., & Yamamoto, N. (2008). Centrifugal innervation of the mammalian olfactory bulb. Anatomical Science International, 83(4), 218–227. https://doi.org/10.1111/j.1447-073x.2007.00223.x

Minces, V., Pinto, L., Dan, Y., & Chiba, A. A. (2017). Cholinergic shaping of neural correlations. Proceedings of the National Academy of Sciences of the United States of America, 114(22), 5725–5730. https://doi.org/10.1073/pnas.1621493114
Miura, K., Mainen, Z. F., & Uchida, N. (2012). Odor Representations in Olfactory Cortex: Distributed Rate Coding and Decorrelated Population Activity. Neuron, 74(6), 1087–1098. https://doi.org/10.1016/j.neuron.2012.04.021
Moyano, H. F., & Molina, J. C. (1982). Olfactory connections of substantia innominata and nucleus of the horizontal limb of the diagonal band in the rat: An electrophysiological study. Neuroscience Letters, 34(3), 241–246. https://doi.org/10.1016/0304-3940(82)90182-3
Murphy, C. M., Christakou, A., Daly, E. M., Ecker, C., Giampietro, V., Brammer, M., Smith, A. B., Johnston, P., Robertson, D. M., Murphy, D. G., Rubia, K., Bailey, A. J., Baron-Cohen, S., Bolton, P. F., Bullmore, E. T., Carrington, S., Chakrabarti, B., Deoni, S. C., Happe, F., … Williams, S. C. (2014). Abnormal functional activation and maturation of fronto-striato-temporal and cerebellar regions during sustained attention in autism spectrum disorder. American Journal of Psychiatry, 171(10), 1107–1116. https://doi.org/10.1176/appi.ajp.2014.12030352
Murphy, D., Critchley, H., Schmitz, N., McAlonan, G., van Amelsvoort, T., Robertson, D., Daly, E., Rowe, A., Russell, A., Simmons, A., Murphy, K., & Howlin, P. (2002). Asperger Syndrome: A Proton Magnetic Resonance Spectroscopy Study of Brain. Archives of General Psychiatry, 59(10), 885–891. https://doi.org/10.1001/archpsyc.59.10.885
Nagayama, S., Enerva, A., Fletcher, M. L., Masurkar, A. V., Igarashi, K. M., Mori, K., & Chen, W. R. (2010). Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Frontiers in Neural Circuits, 4, 1–8. https://doi.org/10.3389/fncir.2010.00120
Nobre, A., Correa, A., & Coull, J. (2007). The hazards of time. Current Opinion in Neurobiology, 17(4), 465–470. https://doi.org/10.1016/j.conb.2007.07.006
Nunez-Parra, A., Cea-Del Rio, C. A., Huntsman, M. M., & Restrepo, D. (2020). The Basal Forebrain Modulates Neuronal Response in an Active Olfactory Discrimination Task. Frontiers in Cellular Neuroscience, 14(June), 1–14. https://doi.org/10.3389/fncel.2020.00141
Nunez-Parra, A., Li, A., & Restrepo, D. (2014). Coding odor identity and odor value in awake rodents. Progress in Brain Research, 208, 205–222. https://doi.org/10.1016/B978-0-444-63350-7.00008-5
Nunez-Parra, A., Maurer, R. K., Krahe, K., Smith, R. S., & Araneda, R. C. (2013). Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proceedings of the National Academy of Sciences of the United States of America, 110(36), 14777–14782. https://doi.org/10.1073/pnas.1310686110
Nusser, Z., Kay, L. M., Laurent, G., Homanics, G. E., & Mody, I. (2001). Disruption of GABAA receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. Journal of Neurophysiology, 86(6), 2823–2833. https://doi.org/10.1152/jn.2001.86.6.2823
Ogg, M. C., Ross, J. M., Bendahmane, M., & Fletcher, M. L. (2018). Olfactory bulb acetylcholine release dishabituates odor responses and reinstates odor investigation. Nature Communications, 9(1), 1868. https://doi.org/10.1038/s41467-018-04371-w
Oikonomakis, V., Kosma, K., Mitrakos, A., Sofocleous, C., Pervanidou, P., Syrmou, A., Pampanos, A., Psoni, S., Fryssira, H., Kanavakis, E., Kitsiou-Tzeli, S., & Tzetis, M. (2016). Recurrent copy number variations as risk factors for autism spectrum disorders: Analysis of the clinical implications. Clinical Genetics, 89(6), 708–718. https://doi.org/10.1111/cge.12740
Okumura, T., Kumazaki, H., Singh, A. K., Touhara, K., & Okamoto, M. (2020). Individuals with Autism Spectrum Disorder Show Altered Event-Related Potentials in the Late Stages of Olfactory Processing. Chemical Senses, 45(1), 45–58. https://doi.org/10.1093/chemse/bjz070
Olender, T., Waszak, S. M., Viavant, M., Khen, M., Ben-Asher, E., Reyes, A., Nativ, N., Wysocki, C. J., Ge, D., & Lancet, D. (2012). Personal receptor repertoires: olfaction as a model. BMC Genomics, 13(1). https://doi.org/10.1186/1471-2164-13-414
Olincy, A., Blakeley-Smith, A., Johnson, L., Kem, W. R., & Freedman, R. (2016). Brief Report: Initial Trial of Alpha7-Nicotinic Receptor Stimulation in Two Adult Patients with Autism Spectrum Disorder. Journal of Autism and Developmental Disorders, 46(12), 3812–3817. https://doi.org/10.1007/s10803-016-2890-6
Oswald, A. M., & Urban, N. N. (2012). There and Back Again: The Corticobulbar Loop. Neuron, 76(6), 1045–1047. https://doi.org/10.1016/j.neuron.2012.12.006
Pashkovski, S. L., Iurilli, G., Brann, D., Chicharro, D., Drummey, K., Franks, K., Panzeri, S., & Datta, S. R. (2020). Structure and flexibility in cortical representations of odour space. Nature, 583(7815), 253–258. https://doi.org/10.1038/s41586-020-2451-1
Patil, M. M., Linster, C., Lubenov, E., & Hasselmo, M. E. (1998). Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. Journal of Neurophysiology, 80(5), 2467–2474. https://doi.org/10.1152/jn.1998.80.5.2467
Perry, E. K., Lee, M. L. W., Martin-Ruiz, C. M., Court, J. A., Volsen, S. G., Merrit, J., Folly, E., Iversen, P. E., Bauman, M. L., Perry, R. H., & Wenk, G. L. (2001). Cholinergic activity in autism: Abnormalities in the cerebral cortex and basal forebrain. American Journal of Psychiatry, 158(7), 1058–1066. https://doi.org/10.1176/appi.ajp.158.7.1058
Petreanu, L., & Alvarez-Buylla, A. (2002). Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction. The Journal of Neuroscience, 22(14), 6106 LP – 6113. https://doi.org/10.1523/JNEUROSCI.22-14-06106.2002
Pinto, L., Goard, M. J., Estandian, D., Xu, M., Kwan, A. C., Lee, S. H., Harrison, T. C., Feng, G., & Dan, Y. (2013). Fast modulation of visual perception by basal forebrain cholinergic neurons. Nature Neuroscience, 16(12), 1857–1863. https://doi.org/10.1038/nn.3552
Price, J. L. (1973). An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. Journal of Comparative Neurology, 150(1), 87–108. https://doi.org/10.1002/cne.901500105
Quast, K. B., Ung, K., Froudarakis, E., Huang, L., Herman, I., Addison, A. P., Ortiz-Guzman, J., Cordiner, K., Saggau, P., Tolias, A. S., & Arenkiel, B. R. (2017). Developmental broadening of inhibitory sensory maps. Nature Neuroscience, 20(2), 189–199. https://doi.org/10.1038/nn.4467
Rajkowski, J., Majczynski, H., Clayton, E., & Aston-Jones, G. (2004). Activation of monkey locus coeruleus neurons varies with difficulty and performance in a target detection task. Journal of Neurophysiology, 92(1), 361–371. https://doi.org/10.1152/jn.00673.2003
Rall, W., Shepherd, G. M., Reese, T. S., & Brightman, M. W. (1966). Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Experimental Neurology, 14(1), 44–56. https://doi.org/10.1016/0014-4886(66)90023-9
Rauss, K., & Pourtois, G. (2013). What is bottom-up and what is top-down in predictive coding. Frontiers in Psychology, 4(MAY), 1–8. https://doi.org/10.3389/fpsyg.2013.00276
Ressler, K. J., Sullivan, S. L., & Buck, L. B. (1994). A molecular dissection of spatial patterning in the olfactory system. Current Opinion in Neurobiology, 4(4), 588–596. https://doi.org/10.1016/0959-4388(94)90061-2
Richardson, R. T., & DeLong, M. R. (1990). Context-dependent responses of primate nucleus basalis neurons in a go/no-go task. Journal of Neuroscience, 10(8), 2528–2540. https://doi.org/10.1523/jneurosci.10-08-02528.1990
Riva, D., Bulgheroni, S., Aquino, D., Di Salle, F., Savoiardo, M., & Erbetta, A. (2011). Basal forebrain involvement in low-functioning autistic children: A voxel-based morphometry study. American Journal of Neuroradiology, 32(8), 1430–1435. https://doi.org/10.3174/ajnr.A2527
Robertson, C. E., & Baron-Cohen, S. (2017). Sensory perception in autism. Nature Reviews Neuroscience, 18(11), 671–684. https://doi.org/10.1038/nrn.2017.112
Robinson, L., Platt, B., & Riedel, G. (2011). Involvement of the cholinergic system in conditioning and perceptual memory. Behavioural Brain Research, 221(2), 443–465. https://doi.org/10.1016/j.bbr.2011.01.055
Roman, F. S., Simonetto, I., & Soumireu-Mourat, B. (1993). Learning and Memory of Odor-Reward Association: Selective Impairment Following Horizontal Diagonal Band Lesions. Behavioral Neuroscience, 107(1), 72–81. https://doi.org/10.1037/0735-7044.107.1.72
Rosin, J. F., Datiche, F., & Cattarelli, M. (1999). Modulation of the piriform cortex activity by the basal forebrain: An optical recording study in the rat. Brain Research, 820(1–2), 105–111. https://doi.org/10.1016/S0006-8993(98)01369-9
Rothermel, M., Carey, R. M., Puche, A., Shipley, M. T., & Wachowiak, M. (2014). Cholinergic inputs from basal forebrain add an excitatory bias to odor coding in the olfactory bulb. Journal of Neuroscience, 34(13), 4654–4664. https://doi.org/10.1523/JNEUROSCI.5026-13.2014
Saar, D., Dadon, M., Leibovich, M., Sharabani, H., Grossman, Y., & Heldman, E. (2007). Opposing effects on muscarinic acetylcholine receptors in the piriform cortex of odor-trained rats. Learning and Memory, 14(3), 224–228. https://doi.org/10.1101/lm.452307
Saar, D., Grossman, Y., & Barkai, E. (2001). Long-lasting cholinergic modulation underlies rule learning in rats. Journal of Neuroscience, 21(4), 1385–1392. https://doi.org/10.1523/jneurosci.21-04-01385.2001
Salcedo, E., Tran, T., Ly, X., Lopez, R., Barbica, C., Restrepo, D., & Vijayaraghavan, S. (2011). Activity-dependent changes in cholinergic innervation of the mouse olfactory bulb. PLoS ONE, 6(10), e25441. https://doi.org/10.1371/journal.pone.0025441
Sanz Diez, A., Najac, M., & De Saint Jan, D. (2019). Basal forebrain GABAergic innervation of olfactory bulb periglomerular interneurons. Journal of Physiology, 597(9), 2547–2563. https://doi.org/10.1113/JP277811
Saper, C. B. (1984). Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. Journal of Comparative Neurology, 222(3), 313–342. https://doi.org/10.1002/cne.902220302
Saper, C. B. (1987). Diffuse Cortical Projection Systems: Anatomical Organization and Role in Cortical Function. Comprehensive Physiology, 217, 169–210. https://doi.org/10.1002/cphy.cp010506
Schoppa, N. E., Kinzie, J. M., Sahara, Y., Segerson, T. P., & Westbrook, G. L. (1998). Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. Journal of Neuroscience, 18(17), 6790–6802. https://doi.org/10.1523/jneurosci.18-17-06790.1998
Semba, K. (2000). Multiple output pathways of the basal forebrain: Organization, chemical heterogeneity, and roles in vigilance. Behavioural Brain Research, 115(2), 117–141. https://doi.org/10.1016/S0166-4328(00)00254-0
Senut, M. C., Menetrey, D., & Lamour, Y. (1989). Cholinergic and peptidergic projections from the medial septum and the nucleus of the diagonal band of broca to dorsal hippocampus, cingulate cortex and olfactory bulb: A combined wheatgerm agglutinin-apohorseradish peroxidase-gold immunohistochemical stu. Neuroscience, 30(2), 385–403. https://doi.org/10.1016/0306-4522(89)90260-1
Shah, A., & Frith, U. (1983). an Islet of Ability in Autistic Children: a Research Note. Journal of Child Psychology and Psychiatry, 24(4), 613–620. https://doi.org/10.1111/j.1469-7610.1983.tb00137.x
Shao, Z., Puche, A. C., Kiyokage, E., Szabo, G., & Shipley, M. T. (2009). Two GABAergic intraglomerular circuits differentially regulate tonic and phasic presynaptic inhibition of olfactory nerve terminals. Journal of Neurophysiology, 101(4), 1988–2001. https://doi.org/10.1152/jn.91116.2008
Shepherd, G. M., Chen, W. R., Willhite, D., Migliore, M., & Greer, C. A. (2007). The olfactory granule cell: From classical enigma to central role in olfactory processing. Brain Research Reviews, 55(2), 373–382. https://doi.org/10.1016/j.brainresrev.2007.03.005
Shi, Y. F., Han, Y., Su, Y. T., Yang, J. H., & Yu, Y. Q. (2015). Silencing of cholinergic basal forebrain neurons using archaerhodopsin prolongs slow-wave sleep in mice. PLoS ONE, 10(7), 1–18. https://doi.org/10.1371/journal.pone.0130130
Shipley, M. T., & Adamek, G. D. (1984). the connections of the mouse olfactory bulb: A study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Research Bulletin, 12(6), 669–688. https://doi.org/10.1016/0361-9230(84)90148-5
Slotnick, B., & Weiler, E. (2009). Olfactory Perception. In M. D. Binder, N. Hirokawa, & U. Windhorst (Eds.), Encyclopedia of Neuroscience (pp. 3007–3010). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-540-29678-2_4192
Smith, R. S., & Araneda, R. C. (2010). Cholinergic modulation of neuronal excitability in the accessory olfactory bulb. Journal of Neurophysiology, 104(6), 2963–2974. https://doi.org/10.1152/jn.00446.2010
Smith, R. S., Hu, R., DeSouza, A., Eberly, C. L., Krahe, K., Chan, W., & Araneda, R. C. (2015). Differential muscarinic modulation in the olfactory bulb. Journal of Neuroscience, 35(30), 10773–10785. https://doi.org/10.1523/JNEUROSCI.0099-15.2015
Soucy, E. R., Albeanu, D. F., Fantana, A. L., Murthy, V. N., & Meister, M. (2009). Precision and diversity in an odor map on the olfactory bulb. Nature Neuroscience, 12(2), 210–220. https://doi.org/10.1038/nn.2262
Soudry, Y., Lemogne, C., Malinvaud, D., Consoli, S. M., & Bonfils, P. (2011). Olfactory system and emotion: Common substrates. European Annals of Otorhinolaryngology, Head and Neck Diseases, 128(1), 18–23. https://doi.org/10.1016/j.anorl.2010.09.007
Spors, H., & Grinvald, A. (2002). Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron, 34(2), 301–315. https://doi.org/10.1016/S0896-6273(02)00644-X
Steriade, M. (2004). Acetylcholine systems and rhythmic activities during the waking-sleep cycle. Progress in Brain Research, 145, 179–196. https://doi.org/10.1016/S0079-6123(03)45013-9
Stevenson, R. A., Philipp-Muller, A., Hazlett, N., Wang, Z. Y., Luk, J., Lee, J., Black, K. R., Yeung, L. K., Shafai, F., Segers, M., Feber, S., & Barense, M. D. (2019). Conjunctive visual processing appears abnormal in Autism. Frontiers in Psychology, 9, 1–7. https://doi.org/10.3389/fpsyg.2018.02668
Suzuki, K., Sugihara, G., Ouchi, Y., Nakamura, K., Tsujii, M., Futatsubashi, M., Iwata, Y., Tsuchiya, K. J., Matsumoto, K., Takebayashi, K., Wakuda, T., Yoshihara, Y., Suda, S., Kikuchi, M., Takei, N., Sugiyama, T., Irie, T., & Mori, N. (2011). Reduced acetylcholinesterase activity in the fusiform gyrus in adults with autism spectrum disorders (Archives of General Psychiatry (2011) 68, 3 (306-313)). Archives of General Psychiatry, 68(5), 306–313. https://doi.org/10.1001/archgenpsychiatry.2011.33
Suzuki, Y., Critchley, H. D., Rowe, A., Howlin, P., & Murphy, D. G. M. (2003). Impaired olfactory identification in Asperger’s syndrome. Journal of Neuropsychiatry and Clinical Neurosciences, 15(1), 105–107. https://doi.org/10.1176/jnp.15.1.105
Tan, J., Savigner, A., Ma, M., & Luo, M. (2010). Odor Information Processing by the Olfactory Bulb Analyzed in Gene-Targeted Mice. Neuron, 65(6), 912–926. https://doi.org/10.1016/j.neuron.2010.02.011
Thomas, A. P., & Westrum, L. E. (1989). Plasticity-related binding of GABA and muscarinic receptor sites in piriform cortex of rat: An autoradiographic study. Experimental Neurology, 105(3), 265–271. https://doi.org/10.1016/0014-4886(89)90129-5
Thomson, E., Lou, J., Sylvester, K., McDonough, A., Tica, S., & Nicolelis, M. A. (2014). Basal forebrain dynamics during a tactile discrimination task. Journal of Neurophysiology, 112(5), 1179–1191. https://doi.org/10.1152/jn.00040.2014
Uchida, N., Poo, C., & Haddad, R. (2014). Coding and transformations in the olfactory system. Annual Review of Neuroscience, 37, 363–385. https://doi.org/10.1146/annurev-neuro-071013-013941
Uchida, N., Takahashi, Y. K., Tanifuji, M., & Mori, K. (2000). Odor maps in the mammalian olfactory bulb: Domain organization and odorant structural features. Nature Neuroscience, 3(10), 1035–1043. https://doi.org/10.1038/79857
van Hoorn, A., Carpenter, T., Oak, K., Laugharne, R., Ring, H., & Shankar, R. (2019). Neuromodulation of autism spectrum disorders using vagal nerve stimulation. Journal of Clinical Neuroscience : Official Journal of the Neurosurgical Society of Australasia, 63, 8–12. https://doi.org/10.1016/j.jocn.2019.01.042
Vassar, R., Chao, S. K., Sitcheran, R., Nuiiez, M., Vosshall, L. B., & Axel, R. (1994). Topographic O rganization of Sensory Projection to the O lfactory Bulb. Cell, 79(6), 981–991. https://doi.org/10.1016/0092-8674(94)90029-9
Villar, P. S., Hu, R., & Araneda, R. C. (2021). Long-Range GABAergic Inhibition Modulates Spatiotemporal Dynamics of the Output Neurons in the Olfactory Bulb. The Journal of Neuroscience, 41(16), 3610–3621. https://doi.org/10.1523/jneurosci.1498-20.2021
Voytko, M. Lou, Olton, D. S., Richardson, R. T., Gorman, L. K., Tobin, J. R., & Price, D. L. (1994). Basal forebrain lesions in monkeys disrupt attention but not learning and memory. Journal of Neuroscience, 14(1), 167–186. https://doi.org/10.1523/jneurosci.14-01-00167.1994
Wang, L., Almeida, L. E. F., Spornick, N. A., Kenyon, N., Kamimura, S., Khaibullina, A., Nouraie, M., & Quezado, Z. M. N. (2015). Modulation of social deficits and repetitive behaviors in a mouse model of autism: The role of the nicotinic cholinergic system. Psychopharmacology, 232(23), 4303–4316. https://doi.org/10.1007/s00213-015-4058-z
Wegiel, J., Flory, M., Kuchna, I., Nowicki, K., Ma, S. Y., Imaki, H., Wegiel, J., Cohen, I. L., London, E., Brown, W. T., & Wisniewski, T. (2014). Brain-region-specific alterations of the trajectories of neuronal volume growth throughout the lifespan in autism. Acta Neuropathologica Communications, 2(1), 1–18. https://doi.org/10.1186/2051-5960-2-28
Wesson, D. W., & Wilson, D. A. (2011). Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics, sensory integration, and more? Neuroscience and Biobehavioral Reviews, 35(3), 655–668. https://doi.org/10.1016/j.neubiorev.2010.08.004
Wilson, C. D., Serrano, G. O., Koulakov, A. A., & Rinberg, D. (2017). A primacy code for odor identity. Nature Communications, 8(1), 1477. https://doi.org/10.1038/s41467-017-01432-4
Wilson, D., & Sullivan, R. (2011). Cortical processing of odor objects. Neuron, 72(4), 506–519. https://doi.org/10.1016/j.neuron.2011.10.027
Wilson, F. A. W., & Rolls, E. T. (1990). Learning and memory is reflected in the responses of reinforcement-related neurons in the primate basal forebrain. Journal of Neuroscience, 10(4), 1254–1267. https://doi.org/10.1523/jneurosci.10-04-01254.1990
Xiong, W., & Chen, W. R. (2002). Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron, 34(1), 115–126. https://doi.org/10.1016/S0896-6273(02)00628-1
Yamaguchi, M., & Mori, K. (2005). Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9697–9702. https://doi.org/10.1073/pnas.0406082102
Yang, C., McKenna, J. T., Zant, J. C., Winston, S., Basheer, R., & Brown, R. E. (2014). Cholinergic neurons excite cortically projecting basal forebrain GABAergic neurons. Journal of Neuroscience, 34(8), 2832–2844. https://doi.org/10.1523/JNEUROSCI.3235-13.2014
Yang, C., Thankachan, S., McCarley, R. W., & Brown, R. E. (2017). The menagerie of the basal forebrain: how many (neural) species are there, what do they look like, how do they behave and who talks to whom? Current Opinion in Neurobiology, 44, 159–166. https://doi.org/10.1016/j.conb.2017.05.004
Yokoi, M., Mori, K., & Nakanishi, S. (1995). Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proceedings of the National Academy of Sciences of the United States of America, 92(8), 3371–3375. https://doi.org/10.1073/pnas.92.8.3371
Yu, J., & Frank, L. (2015). Hippocampal-cortical interaction in decision making. Neurobiology of Learning and Memory, 117, 34–41. https://doi.org/10.1016/j.nlm.2014.02.002
Yu, L., & Wang, S. (2021). Aberrant auditory system and its developmental implications for autism. Science China Life Sciences, 64(6), 861–878. https://doi.org/10.1007/s11427-020-1863-6
Záborszky, L., Carlsen, J., Brashear, H. R., & Heimer, L. (1986a). Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. Journal of Comparative Neurology, 243(4), 488–509. https://doi.org/10.1002/cne.902430405
Záborszky, L., Heimer, L., Eckenstein, F., & Leranth, C. (1986b). GABAergic input to cholinergic forebrain neurons: An ultrastructural study using retrograde tracing of HRP and double immunolabeling. Journal of Comparative Neurology, 250(3), 282–295. https://doi.org/10.1002/cne.902500303Zaborszky, L., & Duque, A. (2000). Local synaptic connections of basal forebrain neurons. Behavioural Brain Research, 115(2), 143–158. https://doi.org/10.1016/S0166-4328(00)00255-2
Zaborszky, L., & Duque, A. (2000). Local synaptic connections of basal forebrain neurons. Behavioural Brain Research, 115(2), 143–158. https://doi.org/10.1016/S0166-4328(00)00255-2Zaborszky, L. (2002). The modular organization of brain systems. Basal forebrain: The last frontier. Progress in Brain Research, 136, 359–372. https://doi.org/10.1016/S0079-6123(02)36030-8
Zaborszky, L., van den Pol, A. N., & Gyengesi, E. (2012). The Basal Forebrain Cholinergic Projection System in Mice. In The Mouse Nervous System. https://doi.org/10.1016/B978-0-12-369497-3.10028-7
Zaborszky, L., Csordas, A., Mosca, K., Kim, J., Gielow, M. R., Vadasz, C., & Nadasdy, Z. (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. Cerebral Cortex, 25(1), 118–137. https://doi.org/10.1093/cercor/bht210
Zaborszky, L., & Gombkoto, P. (2018). The Cholinergic Multicompartmental Basal Forebrain Microcircuit. In G. M. Shepherd, S. Grillner, G. M. Shepherd, & S. Grillner (Eds.), Handbook of Brain Microcircuits (2nd ed., pp. 163–184). Oxford University Press. https://doi.org/10.1093/med/9780190636111.003.0015
Záborszky, L., Gombkoto, P., Varsanyi, P., Gielow, M. R., Poe, G., Role, L. W., Ananth, M., Rajebhosale, P., Talmage, D. A., Hasselmo, M. E., Dannenberg, H., Minces, V. H., & Chiba, A. A. (2018). Specific basal forebrain–cortical cholinergic circuits coordinate cognitive operations. Journal of Neuroscience, 38(44), 9446–9458. https://doi.org/10.1523/JNEUROSCI.1676-18.2018
Zheng, Y., Feng, S., Zhu, X., Jiang, W., Wen, P., Ye, F., Rao, X., Jin, S., He, X., & Xu, F. (2018). Different Subgroups of Cholinergic Neurons in the Basal Forebrain Are Distinctly Innervated by the Olfactory Regions and Activated Differentially in Olfactory Memory Retrieval . In Frontiers in Neural Circuits (Vol. 12). https://www.frontiersin.org/articles/10.3389/fncir.2018.00099


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