Input dependent modulation of olfactory bulb activity by HDB GABAergic projections.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
01 07 2020
01 07 2020
Historique:
received:
15
01
2020
accepted:
27
05
2020
entrez:
3
7
2020
pubmed:
3
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Basal forebrain modulation of central circuits is associated with active sensation, attention, and learning. While cholinergic modulations have been studied extensively the effect of non-cholinergic basal forebrain subpopulations on sensory processing remains largely unclear. Here, we directly compare optogenetic manipulation effects of two major basal forebrain subpopulations on principal neuron activity in an early sensory processing area, i.e. mitral/tufted cells (MTCs) in the olfactory bulb. In contrast to cholinergic projections, which consistently increased MTC firing, activation of GABAergic fibers from basal forebrain to the olfactory bulb leads to differential modulation effects: while spontaneous MTC activity is mainly inhibited, odor-evoked firing is predominantly enhanced. Moreover, sniff-triggered averages revealed an enhancement of maximal sniff evoked firing amplitude and an inhibition of firing rates outside the maximal sniff phase. These findings demonstrate that GABAergic neuromodulation affects MTC firing in a bimodal, sensory-input dependent way, suggesting that GABAergic basal forebrain modulation could be an important factor in attention mediated filtering of sensory information to the brain.
Identifiants
pubmed: 32612119
doi: 10.1038/s41598-020-67276-z
pii: 10.1038/s41598-020-67276-z
pmc: PMC7329849
doi:
Substances chimiques
Channelrhodopsins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10696Références
Zaborszky, L., Van den Pol, A. N. & Gyengesi, E. In The Mouse Nervous System (eds C. Watson, G. Paxinos, & L. Puelles) 684-718 (Elsevier, 2012).
Sarter, M., Hasselmo, M. E., Bruno, J. P. & Givens, B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews 48, 98–111 (2005).
doi: 10.1016/j.brainresrev.2004.08.006
Disney, A. A., Aoki, C. & Hawken, M. J. Gain Modulation by Nicotine in Macaque V1. Neuron 56, 701–713, https://doi.org/10.1016/j.neuron.2007.09.034 (2007).
doi: 10.1016/j.neuron.2007.09.034
pubmed: 18031686
pmcid: 2875676
Goard, M. & Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12, 1444–1449 (2009).
doi: 10.1038/nn.2402
Picciotto, M. R., Higley, M. J. & Mineur, Y. S. Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior. Neuron 76, 116–129, https://doi.org/10.1016/j.neuron.2012.08.036 (2012).
doi: 10.1016/j.neuron.2012.08.036
pubmed: 23040810
pmcid: 3466476
Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139–1152, https://doi.org/10.1016/j.cell.2014.01.050 (2014).
doi: 10.1016/j.cell.2014.01.050
pubmed: 24630718
pmcid: 4041382
McGinley, M. J. et al. Waking State: Rapid Variations Modulate Neural and Behavioral Responses. Neuron 87, 1143–1161, https://doi.org/10.1016/j.neuron.2015.09.012 (2015).
doi: 10.1016/j.neuron.2015.09.012
pubmed: 26402600
pmcid: 4718218
Ogg, M. C., Ross, J. M., Bendahmane, M. & Fletcher, M. L. Olfactory bulb acetylcholine release dishabituates odor responses and reinstates odor investigation. Nat Commun 9, 1868, https://doi.org/10.1038/s41467-018-04371-w (2018).
doi: 10.1038/s41467-018-04371-w
pubmed: 29760390
pmcid: 5951802
Thiele, A. & Bellgrove, M. A. Neuromodulation of Attention. Neuron 97, 769–785, https://doi.org/10.1016/j.neuron.2018.01.008 (2018).
doi: 10.1016/j.neuron.2018.01.008
pubmed: 29470969
pmcid: 6204752
Zaborszky, L. et al. Specific Basal Forebrain-Cortical Cholinergic Circuits Coordinate Cognitive Operations. J Neurosci 38, 9446–9458, https://doi.org/10.1523/JNEUROSCI.1676-18.2018 (2018).
doi: 10.1523/JNEUROSCI.1676-18.2018
pubmed: 30381436
pmcid: 6209837
Hangya, B., Ranade, S. P., Lorenc, M. & Kepecs, A. Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback. Cell 162, 1155–1168, https://doi.org/10.1016/j.cell.2015.07.057 (2015).
doi: 10.1016/j.cell.2015.07.057
pubmed: 26317475
pmcid: 4833212
Raver, S. M. & Lin, S. C. Basal forebrain motivational salience signal enhances cortical processing and decision speed. Front Behav Neurosci 9, 277, https://doi.org/10.3389/fnbeh.2015.00277 (2015).
doi: 10.3389/fnbeh.2015.00277
pubmed: 26528157
pmcid: 4600917
Kim, T. et al. Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc Natl Acad Sci USA 112, 3535–3540, https://doi.org/10.1073/pnas.1413625112 (2015).
doi: 10.1073/pnas.1413625112
pubmed: 25733878
Brown, R. E. & McKenna, J. T. Turning a Negative into a Positive: Ascending GABAergic Control of Cortical Activation and Arousal. Front Neurol 6, 135, https://doi.org/10.3389/fneur.2015.00135 (2015).
doi: 10.3389/fneur.2015.00135
pubmed: 26124745
pmcid: 4463930
Lin, S. C., Brown, R. E., Hussain Shuler, M. G., Petersen, C. C. & Kepecs, A. Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition. J Neurosci 35, 13896–13903, https://doi.org/10.1523/JNEUROSCI.2590-15.2015 (2015).
doi: 10.1523/JNEUROSCI.2590-15.2015
pubmed: 26468190
pmcid: 4604228
Gritti, I. et al. 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, 1051–1064, https://doi.org/10.1016/j.neuroscience.2006.09.024 (2006).
doi: 10.1016/j.neuroscience.2006.09.024
pubmed: 17084984
pmcid: 1831828
Henny, P. & Jones, B. E. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 27, 654–670, https://doi.org/10.1111/j.1460-9568.2008.06029.x (2008).
doi: 10.1111/j.1460-9568.2008.06029.x
pubmed: 18279318
pmcid: 2426826
Zaborszky, L. et al. Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb Cortex 25, 118–137, https://doi.org/10.1093/cercor/bht210 (2015).
doi: 10.1093/cercor/bht210
pubmed: 23964066
Yang, C., Thankachan, S., McCarley, R. W. & Brown, R. E. 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? Curr Opin Neurobiol 44, 159–166, https://doi.org/10.1016/j.conb.2017.05.004 (2017).
doi: 10.1016/j.conb.2017.05.004
pubmed: 28538168
pmcid: 5525536
Busse, L. et al. Sensation during Active Behaviors. J Neurosci 37, 10826–10834, https://doi.org/10.1523/JNEUROSCI.1828-17.2017 (2017).
doi: 10.1523/JNEUROSCI.1828-17.2017
pubmed: 29118211
pmcid: 5678015
Li, X. et al. Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons. Proc Natl Acad Sci USA 115, 415–420, https://doi.org/10.1073/pnas.1703601115 (2018).
doi: 10.1073/pnas.1703601115
pubmed: 29259118
Gielow, M. R. & Zaborszky, L. The Input-Output Relationship of the Cholinergic Basal Forebrain. Cell Rep 18, 1817–1830, https://doi.org/10.1016/j.celrep.2017.01.060 (2017).
doi: 10.1016/j.celrep.2017.01.060
pubmed: 28199851
pmcid: 5725195
Gracia-Llanes, F. J. et al. GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb. Neuroscience 170, 913–922 (2010).
doi: 10.1016/j.neuroscience.2010.07.046
Zaborszky, L. et al. In The Rat Nervous System (Fourth Edition) (ed George Paxinos) 491-507 (Academic Press, 2015).
Zaborszky, L., Carlsen, J., Brashear, H. R. & Heimer, L. 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. J Comp Neurol 243, 488–509, https://doi.org/10.1002/cne.902430405 (1986).
doi: 10.1002/cne.902430405
pubmed: 3512629
Shipley, M. T. & Adamek, G. D. The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12, 669–688 (1984).
doi: 10.1016/0361-9230(84)90148-5
Ma, M. & Luo, M. Optogenetic Activation of Basal Forebrain Cholinergic Neurons Modulates Neuronal Excitability and Sensory Responses in the Main Olfactory Bulb. J Neurosci 32, 10105–10116, https://doi.org/10.1523/jneurosci.0058-12.2012 (2012).
doi: 10.1523/jneurosci.0058-12.2012
pubmed: 22836246
pmcid: 6703727
Rothermel, M., Carey, R. M., Puche, A., Shipley, M. T. & Wachowiak, M. Cholinergic Inputs from Basal Forebrain Add an Excitatory Bias to Odor Coding in the Olfactory Bulb. The Journal of Neuroscience 34, 4654–4664, https://doi.org/10.1523/jneurosci.5026-13.2014 (2014).
doi: 10.1523/jneurosci.5026-13.2014
pubmed: 24672011
pmcid: 3965788
Castillo, P. E., Carleton, A., Vincent, J. D. & Lledo, P. M. Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J Neurosci 19, 9180–9191 (1999).
doi: 10.1523/JNEUROSCI.19-21-09180.1999
Pignatelli, A. & Belluzzi, O. Cholinergic Modulation of Dopaminergic Neurons in the Mouse Olfactory Bulb. Chem. Senses 33, 331–338, https://doi.org/10.1093/chemse/bjm091 (2008).
doi: 10.1093/chemse/bjm091
pubmed: 18209017
Bendahmane, M., Ogg, M. C., Ennis, M. & Fletcher, M. L. Increased olfactory bulb acetylcholine bi-directionally modulates glomerular odor sensitivity. Sci Rep 6, 25808, https://doi.org/10.1038/srep25808 (2016).
doi: 10.1038/srep25808
pubmed: 27165547
pmcid: 4863144
Linster, C. & Cleland, T. A. Cholinergic modulation of sensory representations in the olfactory bulb. Neural Netw 15, 709–717 (2002).
doi: 10.1016/S0893-6080(02)00061-8
Chaudhury, D., Escanilla, O. & Linster, C. Bulbar acetylcholine enhances neural and perceptual odor discrimination. J Neurosci 29, 52–60 (2009).
doi: 10.1523/JNEUROSCI.4036-08.2009
de Almeida, L., Idiart, M. & Linster, C. A model of cholinergic modulation in olfactory bulb and piriform cortex. Journal of Neurophysiology 109, 1360–1377, https://doi.org/10.1152/jn.00577.2012 (2013).
doi: 10.1152/jn.00577.2012
pubmed: 23221406
Devore, S. & Linster, C. Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front Behav Neurosci 6, 52, https://doi.org/10.3389/fnbeh.2012.00052 (2012).
doi: 10.3389/fnbeh.2012.00052
pubmed: 22905025
pmcid: 3417301
Mandairon, N. et al. Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. European Journal of Neuroscience 24, 3234–3244, https://doi.org/10.1111/j.1460-9568.2006.05212.x (2006).
doi: 10.1111/j.1460-9568.2006.05212.x
pubmed: 17156384
Fletcher, M. L. & Wilson, D. A. Experience modifies olfactory acuity: acetylcholine-dependent learning decreases behavioral generalization between similar odorants. J Neurosci 22, RC201 (2002).
doi: 10.1523/JNEUROSCI.22-02-j0005.2002
Liu, S. et al. Muscarinic receptors modulate dendrodendritic inhibitory synapses to sculpt glomerular output. J Neurosci 35, 5680–5692, https://doi.org/10.1523/JNEUROSCI.4953-14.2015 (2015).
doi: 10.1523/JNEUROSCI.4953-14.2015
pubmed: 25855181
pmcid: 4388926
D’Souza, R. D., Parsa, P. V. & Vijayaraghavan, S. Nicotinic receptors modulate olfactory bulb external tufted cells via an excitation-dependent inhibitory mechanism. Journal of Neurophysiology 110, 1544–1553, https://doi.org/10.1152/jn.00865.2012 (2013).
doi: 10.1152/jn.00865.2012
pubmed: 23843430
pmcid: 4042413
Ghatpande, A. S. & Gelperin, A. Presynaptic Muscarinic Receptors Enhance Glutamate Release at the Mitral/Tufted to Granule Cell Dendrodendritic Synapse in the Rat Main Olfactory Bulb. J Neurophysiol 101, 2052–2061, https://doi.org/10.1152/jn.90734.2008 (2009).
doi: 10.1152/jn.90734.2008
pubmed: 19225175
Ravel, N. & Pager, J. Respiratory patterning of the rat olfactory bulb unit activity: nasal versus tracheal breathing. Neurosci Lett 115, 213–218 (1990).
doi: 10.1016/0304-3940(90)90457-K
D’Souza, R. D. & Vijayaraghavan, S. Nicotinic Receptor-Mediated Filtering of Mitral Cell Responses to Olfactory Nerve Inputs Involves the α3β4 Subtype. The Journal of Neuroscience 32, 3261–3266, https://doi.org/10.1523/jneurosci.5024-11.2012 (2012).
doi: 10.1523/jneurosci.5024-11.2012
pubmed: 22378897
pmcid: 3306821
Li, G. & Cleland, T. A. A Two-Layer Biophysical Model of Cholinergic Neuromodulation in Olfactory Bulb. The Journal of Neuroscience 33, 3037–3058, https://doi.org/10.1523/jneurosci.2831-12.2013 (2013).
doi: 10.1523/jneurosci.2831-12.2013
pubmed: 23407960
pmcid: 3711624
Ross, J. M., Bendahmane, M. & Fletcher, M. L. Olfactory Bulb Muscarinic Acetylcholine Type 1 Receptors Are Required for Acquisition of Olfactory Fear Learning. Frontiers in Behavioral Neuroscience 13, https://doi.org/10.3389/fnbeh.2019.00164 (2019).
Zheng, Y. et al. Different Subgroups of Cholinergic Neurons in the Basal Forebrain Are Distinctly Innervated by the Olfactory Regions and Activated Differentially in Olfactory Memory Retrieval. Front Neural Circuits 12, 99, https://doi.org/10.3389/fncir.2018.00099 (2018).
doi: 10.3389/fncir.2018.00099
pubmed: 30483067
pmcid: 6243045
Soma, S., Shimegi, S., Suematsu, N. & Sato, H. Cholinergic modulation of response gain in the rat primary visual cortex. Sci Rep 3, 1138, https://doi.org/10.1038/srep01138 (2013).
doi: 10.1038/srep01138
pubmed: 23378897
pmcid: 3560357
Nunez-Parra, A., Maurer, R. K., Krahe, K., Smith, R. S. & Araneda, R. C. Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proc Natl Acad Sci USA 110, 14777–14782, https://doi.org/10.1073/pnas.1310686110 (2013).
doi: 10.1073/pnas.1310686110
pubmed: 23959889
Sanz Diez, A., Najac, M. & De Saint Jan, D. Basal forebrain GABAergic innervation of olfactory bulb periglomerular interneurons. J Physiol 597, 2547–2563, https://doi.org/10.1113/JP277811 (2019).
doi: 10.1113/JP277811
pubmed: 30920662
pmcid: 6487930
Rossi, J. et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab 13, 195–204, https://doi.org/10.1016/j.cmet.2011.01.010 (2011).
doi: 10.1016/j.cmet.2011.01.010
pubmed: 21284986
pmcid: 3033043
Taniguchi, H. et al. A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex. Neuron 71, 995–1013, https://doi.org/10.1016/j.neuron.2011.07.026 (2011).
doi: 10.1016/j.neuron.2011.07.026
pubmed: 21943598
pmcid: 3779648
Kalmbach, A., Hedrick, T. & Waters, J. Selective optogenetic stimulation of cholinergic axons in neocortex. Journal of Neurophysiology 107, 2008–2019, https://doi.org/10.1152/jn.00870.2011 (2012).
doi: 10.1152/jn.00870.2011
pubmed: 22236708
pmcid: 3331667
Herman, A. M. et al. A cholinergic basal forebrain feeding circuit modulates appetite suppression. Nature 538, 253–256, https://doi.org/10.1038/nature19789 (2016).
doi: 10.1038/nature19789
pubmed: 27698417
pmcid: 5507212
Macrides, F., Davis, B. J., Youngs, W. M., Nadi, N. S. & Margolis, F. L. Cholinergic and catecholaminergic afferents to the olfactory bulb in the hamster: a neuroanatomical, biochemical, and histochemical investigation. J Comp Neurol 203, 495–514 (1981).
doi: 10.1002/cne.902030311
Durand, M., Coronas, V., Jourdan, F. & Quirion, R. Developmental and aging aspects of the cholinergic innervation of the olfactory bulb. Int J Dev Neurosci 16, 777–785, https://doi.org/10.1016/s0736-5748(98)00087-2 (1998).
doi: 10.1016/s0736-5748(98)00087-2
pubmed: 10198824
Salcedo, E. et al. Activity-dependent changes in cholinergic innervation of the mouse olfactory bulb. PLoS One 6, e25441, https://doi.org/10.1371/journal.pone.0025441 (2011).
doi: 10.1371/journal.pone.0025441
pubmed: 22053179
pmcid: 3203864
Gomez, C. et al. Heterogeneous targeting of centrifugal inputs to the glomerular layer of the main olfactory bulb. Journal of Chemical Neuroanatomy 29, 238–254 (2005).
doi: 10.1016/j.jchemneu.2005.01.005
Carey, R. M. & Wachowiak, M. Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci 31, 10615–10626 (2011).
doi: 10.1523/JNEUROSCI.1805-11.2011
Courtiol, E. et al. Reshaping of bulbar odor response by nasal flow rate in the rat. PLoS One 6, e16445, https://doi.org/10.1371/journal.pone.0016445 (2011).
doi: 10.1371/journal.pone.0016445
pubmed: 21298064
pmcid: 3027679
Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M. & Ma, M. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10, 348–354 (2007).
doi: 10.1038/nn1856
Carey, R. M., Verhagen, J. V., Wesson, D. W., Pirez, N. & Wachowiak, M. Temporal Structure of Receptor Neuron Input to the Olfactory Bulb Imaged in Behaving Rats. J Neurophysiol 101, 1073–1088, https://doi.org/10.1152/jn.90902.2008 (2009).
doi: 10.1152/jn.90902.2008
pubmed: 19091924
Linster, C. & Hasselmo, M. E. Neural activity in the horizontal limb of the diagonal band of broca can be modulated by electrical stimulation of the olfactory bulb and cortex in rats. Neurosci Lett 282, 157–160 (2000).
doi: 10.1016/S0304-3940(00)00885-5
Detari, L. & Vanderwolf, C. H. Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetized rats. Brain Res 437, 1–8 (1987).
doi: 10.1016/0006-8993(87)91521-6
Manns, I. D., Alonso, A. & Jones, B. E. Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. J Neurophysiol 89, 1057–1066, https://doi.org/10.1152/jn.00938.2002 (2003).
doi: 10.1152/jn.00938.2002
pubmed: 12574480
Hassani, O. K., Lee, M. G., Henny, P. & Jones, B. E. Discharge Profiles of Identified GABAergic in Comparison to Cholinergic and Putative Glutamatergic Basal Forebrain Neurons across the Sleep-Wake Cycle. Journal of Neuroscience 29, 11828–11840, https://doi.org/10.1523/Jneurosci.1259-09.2009 (2009).
doi: 10.1523/Jneurosci.1259-09.2009
pubmed: 19776269
Voytko, M. L. et al. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14, 167–186 (1994).
doi: 10.1523/JNEUROSCI.14-01-00167.1994
Martinez, V., Parikh, V. & Sarter, M. Sensitized attentional performance and Fos-immunoreactive cholinergic neurons in the basal forebrain of amphetamine-pretreated rats. Biol Psychiatry 57, 1138–1146, https://doi.org/10.1016/j.biopsych.2005.02.005 (2005).
doi: 10.1016/j.biopsych.2005.02.005
pubmed: 15866553
Fuller, P. M., Sherman, D., Pedersen, N. P., Saper, C. B. & Lu, J. Reassessment of the structural basis of the ascending arousal system. J Comp Neurol 519, 933–956, https://doi.org/10.1002/cne.22559 (2011).
doi: 10.1002/cne.22559
pubmed: 21280045
pmcid: 3119596
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E. & McCarley, R. W. Control of sleep and wakefulness. Physiol Rev 92, 1087–1187, https://doi.org/10.1152/physrev.00032.2011 (2012).
doi: 10.1152/physrev.00032.2011
pubmed: 22811426
pmcid: 3621793
Anaclet, C. et al. Basal forebrain control of wakefulness and cortical rhythms. Nat Commun 6, 8744, https://doi.org/10.1038/ncomms9744 (2015).
doi: 10.1038/ncomms9744
pubmed: 26524973
pmcid: 4659943
Cohen, M. R. & Maunsell, J. H. Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12, 1594–1600, https://doi.org/10.1038/nn.2439 (2009).
doi: 10.1038/nn.2439
pubmed: 19915566
pmcid: 2820564
Pinto, L. et al. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16, 1857–1863, https://doi.org/10.1038/nn.3552 (2013).
doi: 10.1038/nn.3552
pubmed: 24162654
pmcid: 4201942
Chen, N., Sugihara, H. & Sur, M. An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nat Neurosci 18, 892–902, https://doi.org/10.1038/nn.4002 (2015).
doi: 10.1038/nn.4002
pubmed: 25915477
pmcid: 4446146
Runfeldt, M. J., Sadovsky, A. J. & MacLean, J. N. Acetylcholine functionally reorganizes neocortical microcircuits. J Neurophysiol 112, 1205–1216, https://doi.org/10.1152/jn.00071.2014 (2014).
doi: 10.1152/jn.00071.2014
pubmed: 24872527
pmcid: 4122727
Thiele, A., Herrero, J. L., Distler, C. & Hoffmann, K. P. Contribution of cholinergic and GABAergic mechanisms to direction tuning, discriminability, response reliability, and neuronal rate correlations in macaque middle temporal area. J Neurosci 32, 16602–16615, https://doi.org/10.1523/JNEUROSCI.0554-12.2012 (2012).
doi: 10.1523/JNEUROSCI.0554-12.2012
pubmed: 23175816
pmcid: 6621794
Nelson, A. & Mooney, R. The Basal Forebrain and Motor Cortex Provide Convergent yet Distinct Movement-Related Inputs to the Auditory Cortex. Neuron 90, 635–648, https://doi.org/10.1016/j.neuron.2016.03.031 (2016).
doi: 10.1016/j.neuron.2016.03.031
pubmed: 27112494
pmcid: 4866808
Do, J. P. et al. Cell type-specific long-range connections of basal forebrain circuit. Elife 5, https://doi.org/10.7554/eLife.13214 (2016).
Agostinelli, L. J., Geerling, J. C. & Scammell, T. E. Basal forebrain subcortical projections. Brain Struct Funct 224, 1097–1117, https://doi.org/10.1007/s00429-018-01820-6 (2019).
doi: 10.1007/s00429-018-01820-6
pubmed: 30612231
pmcid: 6500474
Hasselmo, M. E. & Schnell, E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14, 3898–3914 (1994).
doi: 10.1523/JNEUROSCI.14-06-03898.1994
Tian, M. K., Bailey, C. D. & Lambe, E. K. Cholinergic excitation in mouse primary vs. associative cortex: region-specific magnitude and receptor balance. Eur J Neurosci 40, 2608–2618, https://doi.org/10.1111/ejn.12622 (2014).
doi: 10.1111/ejn.12622
pubmed: 24827827
pmcid: 4640901
Chaves-Coira, I., Barros-Zulaica, N., Rodrigo-Angulo, M. & Nunez, A. Modulation of Specific Sensory Cortical Areas by Segregated Basal Forebrain Cholinergic Neurons Demonstrated by Neuronal Tracing and Optogenetic Stimulation in Mice. Front Neural Circuits 10, 28, https://doi.org/10.3389/fncir.2016.00028 (2016).
doi: 10.3389/fncir.2016.00028
pubmed: 27147975
pmcid: 4837153
Chaves-Coira, I., Martin-Cortecero, J., Nunez, A. & Rodrigo-Angulo, M. L. Basal Forebrain Nuclei Display Distinct Projecting Pathways and Functional Circuits to Sensory Primary and Prefrontal Cortices in the Rat. Front Neuroanat 12, 69, https://doi.org/10.3389/fnana.2018.00069 (2018).
doi: 10.3389/fnana.2018.00069
pubmed: 30158859
pmcid: 6104178
Chaves-Coira, I., Rodrigo-Angulo, M. L. & Nunez, A. Bilateral Pathways from the Basal Forebrain to Sensory Cortices May Contribute to Synchronous Sensory Processing. Front Neuroanat 12, 5, https://doi.org/10.3389/fnana.2018.00005 (2018).
doi: 10.3389/fnana.2018.00005
pubmed: 29410616
pmcid: 5787133
Case, D. T. et al. Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat Commun 8, 652, https://doi.org/10.1038/s41467-017-00765-4 (2017).
doi: 10.1038/s41467-017-00765-4
pubmed: 28935940
pmcid: 5608700
Foutz, T. J., Arlow, R. L. & McIntyre, C. C. Theoretical principles underlying optical stimulation of a channelrhodopsin-2 positive pyramidal neuron. J Neurophysiol 107, 3235–3245, https://doi.org/10.1152/jn.00501.2011 (2012).
doi: 10.1152/jn.00501.2011
pubmed: 22442566
pmcid: 3378402
Woolf, N. J., Eckenstein, F. & Butcher, L. L. Cholinergic systems in the rat brain: I. projections to the limbic telencephalon. Brain Res Bull 13, 751–784 (1984).
doi: 10.1016/0361-9230(84)90236-3
Carlsen, J., Zaborszky, L. & Heimer, L. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234, 155–167, https://doi.org/10.1002/cne.902340203 (1985).
doi: 10.1002/cne.902340203
pubmed: 3886715
Linster, C., Wyble, B. P. & Hasselmo, M. E. Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. J Neurophysiol 81, 2737–2742 (1999).
doi: 10.1152/jn.1999.81.6.2737
Zimmer, L. A., Ennis, M. & Shipley, M. T. Diagonal band stimulation increases piriform cortex neuronal excitability in vivo. Neuroreport 10, 2101–2105 (1999).
doi: 10.1097/00001756-199907130-00020
Boyd, A. M., Sturgill, J. F., Poo, C. & Isaacson, J. S. Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161–1174, https://doi.org/10.1016/j.neuron.2012.10.020 (2012).
doi: 10.1016/j.neuron.2012.10.020
pubmed: 23259951
pmcid: 3725136
Markopoulos, F., Rokni, D., Gire, D. H. & Murthy, V. N. Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175–1188, https://doi.org/10.1016/j.neuron.2012.10.028 (2012).
doi: 10.1016/j.neuron.2012.10.028
pubmed: 23259952
pmcid: 3530161
Otazu, G. H., Chae, H., Davis, M. B. & Albeanu, D. F. Cortical Feedback Decorrelates Olfactory Bulb Output in Awake Mice. Neuron 86, 1461–1477, https://doi.org/10.1016/j.neuron.2015.05.023 (2015).
doi: 10.1016/j.neuron.2015.05.023
pubmed: 26051422
Gritti, I., Manns, I. D., Mainville, L. & Jones, B. E. Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458, 11–31, https://doi.org/10.1002/cne.10505 (2003).
doi: 10.1002/cne.10505
pubmed: 12577320
McKenna, J. T. et al. Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J Comp Neurol 521, 1225–1250, https://doi.org/10.1002/cne.23290 (2013).
doi: 10.1002/cne.23290
pubmed: 23254904
pmcid: 3627393
Zaborszky, L. & Duque, A. Local synaptic connections of basal forebrain neurons. Behavioural Brain Research 115, 143–158, https://doi.org/10.1016/S0166-4328(00)00255-2 (2000).
doi: 10.1016/S0166-4328(00)00255-2
pubmed: 11000417
Yang, C. et al. Cholinergic Neurons Excite Cortically Projecting Basal Forebrain GABAergic Neurons. The Journal of Neuroscience 34, 2832–2844, https://doi.org/10.1523/jneurosci.3235-13.2014 (2014).
doi: 10.1523/jneurosci.3235-13.2014
pubmed: 24553925
pmcid: 3931499
Dannenberg, H. et al. Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks. J Neurosci 35, 8394–8410, https://doi.org/10.1523/JNEUROSCI.4460-14.2015 (2015).
doi: 10.1523/JNEUROSCI.4460-14.2015
pubmed: 26041909
pmcid: 6605336
Ren, J. et al. Habenula Cholinergic Neurons Corelease Glutamate and Acetylcholine and Activate Postsynaptic Neurons via Distinct Transmission Modes. Neuron 69, 445–452 (2011).
doi: 10.1016/j.neuron.2010.12.038
D’Souza, R. D. & Vijayaraghavan, S. Paying attention to smell: cholinergic signaling in the olfactory bulb. Front Synaptic Neurosci 6, 21, https://doi.org/10.3389/fnsyn.2014.00021 (2014).
doi: 10.3389/fnsyn.2014.00021
pubmed: 25309421
pmcid: 4174753
Lendvai, B. & Vizi, E. S. Nonsynaptic chemical transmission through nicotinic acetylcholine receptors. Physiol Rev 88, 333–349, https://doi.org/10.1152/physrev.00040.2006 (2008).
doi: 10.1152/physrev.00040.2006
pubmed: 18391166
Le Jeune, H., Aubert, I., Jourdan, F. & Quirion, R. Comparative laminar distribution of various autoradiographic cholinergic markers in adult rat main olfactory bulb. Journal of Chemical Neuroanatomy 9, 99–112 (1995).
doi: 10.1016/0891-0618(95)00070-N
Keiger, C. J. & Walker, J. C. Individual variation in the expression profiles of nicotinic receptors in the olfactory bulb and trigeminal ganglion and identification of alpha2, alpha6, alpha9, and beta3 transcripts. Biochem Pharmacol 59, 233–240, https://doi.org/10.1016/s0006-2952(99)00326-3 (2000).
doi: 10.1016/s0006-2952(99)00326-3
pubmed: 10609551
Pressler, R. T., Inoue, T. & Strowbridge, B. W. Muscarinic receptor activation modulates granule cell excitability and potentiates inhibition onto mitral cells in the rat olfactory bulb. J Neurosci 27, 10969–10981 (2007).
doi: 10.1523/JNEUROSCI.2961-07.2007
De Saint Jan, D., Hirnet, D., Westbrook, G. L. & Charpak, S. External Tufted Cells Drive the Output of Olfactory Bulb Glomeruli. J. Neurosci. 29, 2043–2052, https://doi.org/10.1523/jneurosci.5317-08.2009 (2009).
doi: 10.1523/jneurosci.5317-08.2009
Najac, M., De Saint Jan, D., Reguero, L., Grandes, P. & Charpak, S. Monosynaptic and Polysynaptic Feed-Forward Inputs to Mitral Cells from Olfactory Sensory Neurons. The Journal of Neuroscience 31, 8722–8729, https://doi.org/10.1523/jneurosci.0527-11.2011 (2011).
doi: 10.1523/jneurosci.0527-11.2011
pubmed: 21677156
pmcid: 6622927
Gire, D. H. et al. Mitral Cells in the Olfactory Bulb Are Mainly Excited through a Multistep Signaling Path. The Journal of Neuroscience 32, 2964–2975, https://doi.org/10.1523/jneurosci.5580-11.2012 (2012).
doi: 10.1523/jneurosci.5580-11.2012
pubmed: 22378870
pmcid: 3467005
Caputi, A., Melzer, S., Michael, M. & Monyer, H. The long and short of GABAergic neurons. Curr Opin Neurobiol 23, 179–186, https://doi.org/10.1016/j.conb.2013.01.021 (2013).
doi: 10.1016/j.conb.2013.01.021
pubmed: 23394773
Short, S. M. & Wachowiak, M. Temporal dynamics of inhalation-linked activity across defined subpopulations of mouse olfactory bulb neurons imaged in vivo. bioRxiv, 558999, https://doi.org/10.1101/558999 (2019).
Nagayama, S., Homma, R. & Imamura, F. Neuronal organization of olfactory bulb circuits. Front Neural Circuits 8, 98, https://doi.org/10.3389/fncir.2014.00098 (2014).
doi: 10.3389/fncir.2014.00098
pubmed: 25232305
pmcid: 4153298
McDonald, A. J., Muller, J. F. & Mascagni, F. Postsynaptic targets of GABAergic basal forebrain projections to the basolateral amygdala. Neuroscience 183, 144–159, https://doi.org/10.1016/j.neuroscience.2011.03.027 (2011).
doi: 10.1016/j.neuroscience.2011.03.027
pubmed: 21435381
pmcid: 4586026
Kato, H. K., Chu, M. W., Isaacson, J. S. & Komiyama, T. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76, 962–975, https://doi.org/10.1016/j.neuron.2012.09.037 (2012).
doi: 10.1016/j.neuron.2012.09.037
pubmed: 23217744
pmcid: 3523713
Wachowiak, M. et al. Optical Dissection of Odor Information Processing In Vivo Using GCaMPs Expressed in Specified Cell Types of the Olfactory Bulb. J Neurosci 33, 5285–5300, https://doi.org/10.1523/jneurosci.4824-12.2013 (2013).
doi: 10.1523/jneurosci.4824-12.2013
pubmed: 23516293
pmcid: 3690468
Youngstrom, I. A. & Strowbridge, B. W. Respiratory modulation of spontaneous subthreshold synaptic activity in olfactory bulb granule cells recorded in awake, head-fixed mice. J Neurosci 35, 8758–8767, https://doi.org/10.1523/JNEUROSCI.0311-15.2015 (2015).
doi: 10.1523/JNEUROSCI.0311-15.2015
pubmed: 26063910
pmcid: 4461684
Xu, M. et al. Basal forebrain circuit for sleep-wake control. Nat Neurosci 18, 1641–1647, https://doi.org/10.1038/nn.4143 (2015).
doi: 10.1038/nn.4143
pubmed: 26457552
pmcid: 5776144
Harrison, T. C., Pinto, L., Brock, J. R. & Dan, Y. Calcium Imaging of Basal Forebrain Activity during Innate and Learned Behaviors. Front Neural Circuits 10, 36, https://doi.org/10.3389/fncir.2016.00036 (2016).
doi: 10.3389/fncir.2016.00036
pubmed: 27242444
pmcid: 4863728
Paolini, A. G. & McKenzie, J. S. Intracellular recording of magnocellular preoptic neuron responses to olfactory brain. Neuroscience 78, 229–242, https://doi.org/10.1016/s0306-4522(96)00566-0 (1997).
doi: 10.1016/s0306-4522(96)00566-0
pubmed: 9135103
Rothermel, M. & Wachowiak, M. Functional imaging of cortical feedback projections to the olfactory bulb. Front Neural Circuits 8, 73, https://doi.org/10.3389/fncir.2014.00073 (2014).
doi: 10.3389/fncir.2014.00073
pubmed: 25071454
pmcid: 4080262
Bozza, T., McGann, J. P., Mombaerts, P. & Wachowiak, M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42, 9–21 (2004).
doi: 10.1016/S0896-6273(04)00144-8
Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A. & Wachowiak, M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10, 631–639 (2007).
doi: 10.1038/nn1892
Wachowiak, M. & Cohen, L. B. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723–735 (2001).
doi: 10.1016/S0896-6273(01)00506-2
Spors, H., Wachowiak, M., Cohen, L. B. & Friedrich, R. W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26, 1247–1259 (2006).
doi: 10.1523/JNEUROSCI.3100-05.2006
Eiting, T. P. & Wachowiak, M. Artificial Inhalation Protocol in Adult Mice. Bio Protoc 8, https://doi.org/10.21769/BioProtoc.3024 (2018).
Lewicki, M. S. A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9, R53–78 (1998).
doi: 10.1088/0954-898X_9_4_001