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Chapter 11 - The Vibrissa Sensorimotor System of Rodents: A View from the Sensory Thalamus

from Section 5: - Sensory Processing

Published online by Cambridge University Press:  12 August 2022

By
Martin Deschênes  and
David Kleinfeld
Edited by
Michael M. Halassa
Michael M. Halassa
Affiliation:
Massachusetts Institute of Technology
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Summary

The rodent somatic sensory system is characterized by a prominent representation of the mystacial vibrissae, which form an orderly array of low-threshold mechanoreceptors. Centrally, the arrangement of the vibrissal pad is maintained in arrays of cellular aggregates referred to as barrelettes (brainstem), barreloids (thalamus), and barrels (primary sensory cortex). Trigeminal brainstem nuclei that receive vibrissal primary afferents give rise to two main streams of information, the lemniscal and paralemniscal pathways. The lemniscal pathway arises from the trigeminal nucleus principalis, transits through the ventral posterior medial nucleus of the thalamus, and projects to the primary somatosensory cortex. The paralemniscal pathway arises from the rostral part of trigeminal spinal nucleus interpolaris, transits through the posterior group of the thalamus, and projects to the somatosensory cortical areas and the vibrissa motor cortex. In this chapter, we review the anatomical organization of these pathways and propose that whereas the lemniscal pathway encodes both touch and whisking kinematics, the paralemniscal pathway signals the valence of orofacial inputs. Lastly, we call attention to the importance of understanding sensory processing in the brainstem trigeminal nuclei to understand their role in regulating behavior. These nuclei are richly interconnected and contain inhibitory circuits that operate both pre- and postsynaptically.

Keywords

barrelettesbarreloidsbarrelsextralemniscallemniscalparalemniscalself-motiontouchtrigeminuswhisking
Type
Chapter
Information
The Thalamus , pp. 214 - 220
Publisher: Cambridge University Press
Print publication year: 2022

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References

Alloway, KD, Olson, ML, Smith, JB (2008) Contralateral corticothalamic projections from M1 whisker cortex: potential route for modulating hemispheric interactions. J. Comp. Neurol. 510: 100–116.Google Scholar
Alloway, KD, Smith, JB, Watson, GDR (2013) Thalamostriatal projections from the medial posterior and parafascicular nuclei have distinct topographic and physiologic properties. J. Neurophysiol. 111: 36–50.CrossRefGoogle ScholarPubMed
Andermann, ML, Moore, CI (2006) A somatotopic map of vibrissa motion direction within a barrel column. Nat. Neurosci. 9: 543–551.Google Scholar
Armstrong-James, M, Fox, K (1987) Spatiotemporal convergence and divergence in the rat S1 “barrel” cortex. J. Comp. Neurol. 263: 265–281.CrossRefGoogle ScholarPubMed
Arsenault, D, Zhang, ZW (2006) Developmental remodeling of the lemniscal synapse in the ventral basal thalamus of the mouse. J. Physiol. 573: 121–132.CrossRefGoogle ScholarPubMed
Bae, YC, Yoshida, S (2011) Ultrastructure basis for craniofacial sensory processing in the brainstem. Int. Rev. Neurobiol. 97: 99–141.Google Scholar
Barthó, P, Freund, TF, Acsády, L (2002) Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur. J. Neurosci. 16: 999–1014.Google Scholar
Bokor, H, Acsády, L, Deschênes, M (2008) Vibrissal responses of thalamic cells that project to the septal columns of the barrel cortex and to the second somatosensory area. J. Neurosci. 28: 5169–5177.Google Scholar
Bokor, H, Frère, SGA, Eyre, MD, Slézia, A, Ulbert, I, Luthi, A, Acsady, L (2005) Selective GABAergic control of higher thalamic relays. Neuron 45: 929–940.Google Scholar
Bourassa, J, Pinault, D, Deschênes, M (1995) Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur. J. Neurosci. 7: 19–30.CrossRefGoogle Scholar
Brecht, M, Preilowski, B, Merzenich, MM (1997) Functional architecture of the mystacial vibrissae. Behav. Brain Res. 84: 81–97.Google Scholar
Brown, J, Oldenburg, IA, Telia, GI, Griffin, S, Voges, M, Jain, V, Adesnik, H (2021) Spatial integration during active tactile sensation drives orientation perception. Neuron. 107: 1707–1720.CrossRefGoogle Scholar
Brumberg, JC, Pinto, DJ, Simons, DJ (1999) Cortical columnar processing in the rat whisker-to-barrel system. J. Neurophysiol. 82: 1808–1817.Google Scholar
Bruno, RM, Khatri, V, Land, PW, Simons, DJ (2003) Thalamocortical angular tuning domains within individual barrels of rat somatosensory cortex. J. Neurosci. 23: 9565–9574.CrossRefGoogle ScholarPubMed
Castro-Alamancos, MA (2002). Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J. Neurophysiol. 87: 946–953.Google Scholar
Cheung, JA, Maire, P, Kim, J, Lee, K, Flynn, G, Hires, SA (2020) Independent representations of self-motion and object location in barrel cortex output. PLoS Biol. 8:e3000882.CrossRefGoogle Scholar
Curtis, JC, Kleinfeld, D (2009) Phase to rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nat. Neurosci. 12: 492–501.Google Scholar
de Kock, CPJ, Pie, J, Pieneman, AW, Mease, RA, Bast, A, Guest, JM, Oberlaender, M Huibert, D, Mansvelder, HD, Sakmann, B (2021) High-frequency burst spiking in layer 5 thick-tufted pyramids of rat primary somatosensory cortex encodes exploratory touch. Commun. Biol. 4: 709.CrossRefGoogle ScholarPubMed
Deschênes, M, Timofeeva, E, Lavallée, P (2003) The relay of high-frequency signals in the whisker-to-barrel pathway. J. Neurosci. 23: 6778–6787.Google Scholar
Deschênes, M, Urbain, N (2016) Vibrissal afferents from trigeminus to cortices. In Prescott, TJ et al. (eds), Scholarpedia of touch, Atlantis Press, pp. 657–672.CrossRefGoogle Scholar
Deschênes, M, Veinante, P, Zhang, ZW (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Res. Rev. 28: 286–308.Google Scholar
Diamond, ME, Armstrong-James, M, Budway, MJ, Ebner, FF (1992) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: Dependence on the barrel field cortex. J. Comp. Neurol. 319: 66–84.Google Scholar
Elbaz, M, Callado-Pérez, A, Demers, M, Foo, C, Kleinfeld, D, Deschênes, M (2022) A vibrissa pathway that activates the limbic system. eLife. 11: e72096.CrossRefGoogle ScholarPubMed
Frangeul, L, Porrero, C, Garcia-Amado, M, Maimone, B, Maniglier, M, Clascá, F, Jabaudon, D (2014) Specific activation of the paralemniscal pathway during nociception. Eur. J. Neurosci. 39: 1455–1464.Google Scholar
Furuta, T, Deschênes, M, Kaneko, T (2011) Anisotropic distribution of thalamocortical boutons in barrels. J. Neurosci. 31: 6432–6439.CrossRefGoogle ScholarPubMed
Furuta, T, Kaneko, T, Deschênes, M (2009) Septal neurons in barrel cortex derive their receptive field input from the lemniscal pathway. J. Neurosci. 29: 4089–4095.Google Scholar
Furuta, T, Timofeeva, E, Nakamura, K, Okamoto-Furuta, K, Togo, M, Kaneko, T, Deschênes, M (2008) Inhibitory gating of vibrissal inputs in the brainstem. J. Neurosci. 28: 1789–1797.Google Scholar
Geerling, JC, Yokota, S, Rikhadze, I, Roe, D, Chamberlin, NL (2017) Kölliker-Fuse GABAergic and glutamatergic neurons project to distinct targets. J. Comp. Neurol. 525: 1844–1860.Google Scholar
Grant, RA, Sperber, AL, Prescott, TJ (2012) The role of orienting in vibrissal touch sensing. Front. Behav. Neurosci. 6: 39. doi.org/10.3389/fnbeh.2012.00039.Google Scholar
Groenewegen, HJ, Witter, MP (2004) Thalamus. In Paxinos, G (ed), The rat nervous system, 3rd edition, Academic Press, pp. 407–453.Google Scholar
Haidarliu, S, Ahissar, E (2001) Size gradients of barreloids in the rat thalamus. J. Comp. Neurol. 429: 372–387.Google Scholar
Haidarliu, S, Simony, E, Golomb, D, Ahissar, E (2010) Muscle architecture in the mystacial pad of the rat. Anat. Rec. 293: 1192–1206.Google Scholar
Harrell, ER, Renard, A, Bathellier, B (2021) Fast cortical dynamics encode tactile grating orientation during active touch. Sci. Adv. 7. doi.org/10.1126/sciadv.abf7096.Google Scholar
Henderson, TA, Jacquin, MF (1995) What makes subcortical barrels? In Jones, EG and Diamond, IT (eds), Cerebral Cortex, the Barrel Cortex of Rodents, Vol. 11, Plenum, pp. 123–187.Google Scholar
Isett, BR, Feasel, SH, Lane, MA, Feldman, DE (2018) Slip-based coding of local shape and texture in mouse S1. Neuron. 97: 418–433.Google Scholar
Isett, BR, Feldman, DE (2020) Cortical coding of whisking phase during surface whisking. Curr. Biol. 30: 3065–3074.Google Scholar
Ito, M (1988) Response properties and topography of vibrissa-sensitive VPM neurons in the rat. J. Neurophysiol. 60: 1181–1197.Google Scholar
Jacquin, MF, Rhoades, RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens. Mot. Res. 7: 265–288.CrossRefGoogle ScholarPubMed
Jadhav, SP, Wolfe, J, Feldman, DE (2009) Sparse temporal coding of elementary tactile features during active whisker sensation. Nat. Neurosci. 12: 792–800.Google Scholar
Killackey, HP, Sherman, SM (2003) Corticothalamic projections from the rat primary somatosensory cortex. J. Neurosci. 23: 7381–7384.CrossRefGoogle ScholarPubMed
Kleinfeld, D, Deschênes, M (2011) Neuronal basis for object location in the vibrissa scanning sensorimotor system. Neuron 72: 455–468.CrossRefGoogle ScholarPubMed
Kleinfeld, D, Sachdev, RNS, Merchant, LM, Jarvis, MR, Ebner, FF (2002) Adaptive filtering of vibrissa input in motor cortex of rat. Neuron 34:1021–1034.Google Scholar
Knutsen, PM, Pietr, M, Ahissar, E (2006) Haptic object localization in the vibrissal system: behavior and performance. J. Neurosci. 26: 8451–8464.Google Scholar
Kurnikova, A, Moore, JD, Liao, S-M, Deschênes, M, Kleinfeld, D (2017) Coordination of orofacial motor actions into exploratory behavior by rat. Curr. Biol. 27: 688–696.Google Scholar
Kuruppath, P, Gugig, E, Azouz, R (2014) Microvibrissae-based texture discrimination. J. Neurosci. 34: 5115–5120.Google Scholar
Lavallée, P, Urbain, N, Dufresne, C, Bokor, H, Acsády, L, Deschênes, M (2005) Feedforward inhibitory control of sensory information in higher-order thalamic nuclei. J. Neurosci. 25: 7489–7498.Google Scholar
Liu, R, Li, Z, Marvin, JS, Kleinfeld, D (2019) Direct wavefront sensing enables functional imaging of infragranular axons and spines. Nat. Meth. 16: 615–618.CrossRefGoogle ScholarPubMed
Liu, R, Yao, P, Deschênes, M, Kleinfeld, D (2019) Deep layer cortical circuits underlying active sensing revealed by two-photon adaptive optical imaging. Society for Neuroscience Annual Meeting (Chicago) poster 057.06.Google Scholar
Lo, F-S, Guigo, W, Erzurumlu, RS (1999) Electrophysiological properties and synaptic responses of cells in the trigeminal principal sensory nucleus of postnatal rats. J. Neurophysiol. 82: 2765–2775.Google Scholar
Luo, L, Callaway, EM, Svoboda, K (2008) Genetic dissection of neural circuits. Neuron 57: 634–660.Google Scholar
Luo, L, Callaway, EM, Svoboda, K (2018) Genetic dissection of neural circuits: a decade of progress. Neuron 98: 256–281.Google Scholar
Ma, PM, Woolsey, TA (1984) Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. Brain Res. 306: 374–379.Google Scholar
Masri, R, Quiton, RL, Lucas, JM, Murray, PD, Thompson, SM, Keller, A (2009) Zona incerta: a role in central pain. J. Neurophysiol. 102: 181–191.Google Scholar
Metha, SB, Kleinfeld, D (2004) Frisking the whiskers: patterned sensory input in the rat vibrissa system. Neuron 41:181–184.Google Scholar
Metha, SB, Whitmer, D, Figueroa, R, Williams, BA, Kleinfeld, D (2007) Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 5: 309–322.Google Scholar
Minnery, BS, Simons, DJ (2003) Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis. J. Neurophysiol. 89: 40–56.Google Scholar
Moore, JD, Mercer Lindsay, N, Deschênes, M, Kleinfeld, D (2015) Vibrissa self-motion and touch are reliably encoded along the same somatosensory pathway from brainstem through thalamus. PLoS Biol. 13: e1002253.Google Scholar
O’Connor, DH, Clack, NG, Huber, D, Komiyama, T, Myers, EW, Svoboda, K (2010) Vibrissa-based object localization in head-fixed mice. J. Neurosci. 30: 1947–1967.CrossRefGoogle ScholarPubMed
O’Connor, DH, Peron, SP, Huber, D, Svoboda, K (2010) Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67: 1048–1061.Google Scholar
Ohno, S, Kuramoto, E, Furuta, T, Hioki, H, Tanaka, Y-R, Fujiyama, F, Sonomura, T, Uemura, M, Sugiyama, K, Kaneko, T (2012) A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb. Cortex 22: 2840–2857.Google Scholar
Parmiani, P, Lucchette, C, Franchi, G (2018) Whisker and nose tactile sense guide rat behavior in a skilled reaching task. Front. Behav. Neurosci. 12: 24. doi.org/10.3389/fnbeh.2018.00024.Google Scholar
Pierret, T, Lavallée, P, Deschênes, M (2000) Parallel streams for the relay of vibrissal information through thalamic barreloids. J. Neurosci. 20: 7455–7462.Google Scholar
Pinault, D, Bourassa, J, Deschênes, M (1995) The axonal arborization of single thalamic reticular neurons in the somatosensory thalamus of the rat. Eur. J. Neurosci. 7: 31–40.CrossRefGoogle ScholarPubMed
Pouchelon, G, Frangeul, L, Rijli, F-M, Jabaudon, D (2012) Patterning of pre-thalamic somatosensory pathways. Eur. J. Neurosci. 35: 1533–1539.Google Scholar
Prescott, TJ, Diamond, ME, Wing, AM (2011) Active touch sensing. Phil. Trans. Roy. Soc. Lond. Biol. 366: 2989–2995.Google Scholar
Ranganathan, GN, Apostolides, PF, Harnett, MT, Xu, N-L, Druckmann, S, Magee, JC (2018) Active dendritic integration and mixed neocortical network representations during an adaptive sensing behavior. Nat. Neuro. 21: 1583–1590.CrossRefGoogle ScholarPubMed
Renehan, WE, Jacquin, MF, Mooney, RD, Rhoades, RW (1986) Structure-function relationships in rat medullary and cervical dorsal horns. II. Medullary dorsal horn cells. J. Neurophysiol. 55: 1187–1201.Google Scholar
Severson, KS, Xu, D, Van de Loo, M, Bai, L, Ginty, DD, O’Connor, DH (2017) Active touch and self-motion encoding by Merkel cell-associated afferents. Neuron. 94: e669.CrossRefGoogle ScholarPubMed
Severson, KS, Xu, D, Van de Loo, M, Bai, L, Ginty, DD, O’Connor, DH (2017) Active touch and self-motion encoding by Merkel cell-associated afferents. Neuron 94: 666–676.CrossRefGoogle ScholarPubMed
Sosnik, R, Haidarliu, S, Ahissar, E (2001) Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. J. Neurophysiol. 86: 339–353.CrossRefGoogle ScholarPubMed
Spácek, J, Lieberman, AR (1974). Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus. J. Anat. 117: 487–516.Google Scholar
Sugitani, M, Yano, J, Sugai, T, Ooyama, H (1990) Somatotopic organization and columnar structure of vibrissae representation in the rat ventrobasal complex. Exp. Brain Res. 81: 346–352.CrossRefGoogle ScholarPubMed
Szwed, M, Bagdasarian, K, Ahissar, E (2003) Coding of vibrissal active touch. Neuron 40: 621–630.Google Scholar
Timofeeva, E, Mérette, C, Emond, C, Lavallée, P, Deschênes, M (2003) A map of angular tuning preference in thalamic barreloids. J. Neurosci. 23:10717–10723.CrossRefGoogle ScholarPubMed
Trageser, JC, Keller, A (2004) Reducing the uncertainty: gating of peripheral inputs by zona incerta. J. Neurosci. 24: 8911–8915.Google Scholar
Urbain, N, Deschênes, M (2007) A new thalamic pathway of vibrissal information modulated by the motor cortex. J. Neurosci. 27, 12407–12412.Google Scholar
Urbain, N, Salin, PA, Libourel, P-A, Comte, J-C, Gentet, LJ, Petersen, CCH (2015) Whisking-related changes in neuronal firing and membrane potential dynamics in the somatosensory thalamus of awake mice. Cell Rep. 13: 647–656.Google Scholar
Van der Loos, H (1976) Barreloids in the mouse somatosensory. Neurosci. Let. 2: 1–6.Google Scholar
Veinante, P, Deschênes, M (1999) Single- and multi-whisker channels in the ascending projections from the principal trigeminal nucleus in the rat. J. Neurosci. 19: 5085–5095.Google Scholar
Veinante, P, Jacquin, M, Deschênes, M (2000) Thalamic projections from the whisker sensitive regions of the spinal trigeminal complex in the rat. J. Comp. Neurol. 420: 233–240.Google Scholar
Whiteley, SJ, Knutsen, PM, Matthews, DM, Kleinfeld, D (2015) Deflection of a vibrissa leads to a gradient of strain across mechanoreceptors in the mystacial follicle. J. Neurophysiol. 114: 138–145.Google Scholar
Williams, MN, Zahm, DS, Jacquin, MF (1994) Differential foci and synaptic organization of the principal and spinal trigeminal projections to the thalamus in the rat. Eur. J. Neurosci. 6: 429–453.Google Scholar
Wolfe, J, Hill, DN, Pahlavan, S, Drew, PJ, Kleinfeld, D, Feldman, DE (2008) Texture coding in the rat whisker system: Slip-stick versus differential resonance. PLoS Bio. doi.org/10.1371/journal.pbio.0060215.Google Scholar
Woolsey, TA, Van der Loos, H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17: 205–242.Google Scholar
Xu, N-L, Harnett, MT, Williams, SR, Huber, D, O’Connor, DH, Svoboda, K, Magee, JC (2012) Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492: 247–251.Google Scholar
Yu, C, Derdikman, D, Haidarliu, S, Ahissar, E (2006) Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 4: 819–825.Google Scholar

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