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Brain Structure and Function
Published in: Brain Structure and Function 1/2022

01-01-2022 | Original Article

Convergence of forepaw somatosensory and motor cortical projections in the striatum, claustrum, thalamus, and pontine nuclei of cats

Authors: Jared B. Smith, Shubhodeep Chakrabarti, Todd M. Mowery, Kevin D. Alloway

Published in: Brain Structure and Function | Issue 1/2022

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Abstract

The basal ganglia and pontocerebellar systems regulate somesthetic-guided motor behaviors and receive prominent inputs from sensorimotor cortex. In addition, the claustrum and thalamus are forebrain subcortical structures that have connections with somatosensory and motor cortices. Our previous studies in rats have shown that primary and secondary somatosensory cortex (S1 and S2) send overlapping projections to the neostriatum and pontine nuclei, whereas, overlap of primary motor cortex (M1) and S1 was much weaker. In addition, we have shown that M1, but not S1, projects to the claustrum in rats. The goal of the current study was to compare these rodent projection patterns with connections in cats, a mammalian species that evolved in a separate phylogenetic superorder. Three different anterograde tracers were injected into the physiologically identified forepaw representations of M1, S1, and S2 in cats. Labeled fibers terminated throughout the ipsilateral striatum (caudate and putamen), claustrum, thalamus, and pontine nuclei. Digital reconstructions of tracer labeling allowed us to quantify both the normalized distribution of labeling in each subcortical area from each tracer injection, as well as the amount of tracer overlap. Surprisingly, in contrast to our previous findings in rodents, we observed M1 and S1 projections converging prominently in striatum and pons, whereas, S1 and S2 overlap was much weaker. Furthermore, whereas, rat S1 does not project to claustrum, we confirmed dense claustral inputs from S1 in cats. These findings suggest that the basal ganglia, claustrum, and pontocerebellar systems in rat and cat have evolved distinct patterns of sensorimotor cortical convergence.
Literature
Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381PubMed
Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia- thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146PubMed
Alitto HJ, Usrey WM (2003) Corticothalamic feedback and sensory processing. Curr Opin Neurobiol 13:440–445PubMed
Alloway KD (2008) Information processing streams in rodent barrel cortex: the differential functions of barrel and septal circuits. Cereb Cortex 18:979–989PubMed
Alloway KD, Burton H (1985a) Submodality and columnar organization of the second somatic sensory area in cats. Exp Brain Res 61:128–140PubMed
Alloway KD, Burton H (1985b) Homotypical ipsilateral cortical projections between somatosensory areas I and II in the cat. Neuroscience 14:14–35
Alloway KD, Mutic JJ, Hoffer ZS, Hoover JE (2000) Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex. J Comp Neurol 426:51–67PubMed
Alloway KD, Lou L, Nwabueze-Ogbo F, Chakrabarti S (2006) Topography of cortical projections to the dorsolateral neostriatum in rats: multiple overlapping sensorimotor pathways. J Comp Neurol 499:33–48PubMed
Alloway KD, Olson ML, Smith JB (2008) Contralateral corticothalamic projections from MI whisker cortex: potential route for modulating hemispheric interactions. J Comp Neurol 510:100–116PubMedPubMedCentral
Alloway KD, Smith JB, Beauchemin KJ, Olson ML (2009) Bilateral projections from rat MI whisker cortex to the neostriatum, thalamus, and claustrum: forebrain circuits for modulating whisker behavior. J Comp Neurol 515:548–564PubMedPubMedCentral
Alloway KD, Smith JB, Mowery TM, Watson GDR (2017) Sensory processing in the dorsolateral striatum: the contribution of thalamostriatal pathways. Front Syst Neurosci 11:53PubMedPubMedCentral
Aoki S, Coulon P, Ruigrok TJH (2019a) Multizonal cerebellar influence over sensorimotor areas of the rat cerebral cortex. Cereb Cortex 29:598–614PubMed
Arce-McShane FI, Ross CF, Takahashi K, Sessle BJ, Hatsopoulos NG (2016) Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies. Proc Nat Acad Sci USA 113:5083–5088PubMedPubMedCentral
Battaglia-Mayer A, Caminiti R (2019) Corticocortical systems underlying high-order motor control. J Neurosci 39:4404–4421PubMedPubMedCentral
Bjaalie JG, Brodal P (1989) Visual pathways to the cerebellum: segregation in the pontine nuclei of terminal fields from different visual cortical areas in the cat. Neuroscience 29:95–107PubMed
Borich MR, Brodie SM, Gray WA, Ionta S, Boyd LA (2015) Understanding the role of the primary somatosensory cortex: opportunities for rehabilitation. Neuropsycholigia 79:246–255
Briggs F, Usrey WM (2008) Emerging views of corticothalamic function. Curr Opinion Neurobiol 18:403–407
Brodal P (1978) Principles of organization of the monkey corticopontine projection. Brain Res 148:214–218PubMed
Burton H, Mitchell G, Brent S (1982) Second somatic sensory area in the cerebral cortex of cats: somatotopic organization and cytoarchitecture. J Comp Neurol 210:109–135PubMed
Chakrabarti S, Alloway KD (2006) Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI. J Comp Neurol 498:624–636PubMed
Chakrabarti S, Zhang M, Alloway KD (2008) MI neuronal responses to peripheral whisker stimulation: relationship to neuronal activity in SI barrels and septa. J Neurophysiol 100:50–63PubMedPubMedCentral
Chapin JK, Lin CS (1984) Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229:199–213PubMed
Charpier S, Pidoux M, Mahon S (2020) Converging sensory and motor cortical inputs onto the same striatal neurons: an in vivo intracellular investigation. PLoS ONE 15(2):e0228260PubMedPubMedCentral
Chen S, Augustine GJ, Chadderton P (2016) The cerebellum linearly encodes whisker position during voluntary movement. Elife 5:e10509PubMedPubMedCentral
Colechio EM, Alloway KD (2009) Differential topography of the bilateral cortical projections to the whisker and forepaw regions in rat motor cortex. Brain Struct Funct 213:423–439PubMed
Doyon J, Penhune V, Ungerleider LG (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41:252–262PubMed
Dudman JT, Gerfen CR (2015) The basal ganglia. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, San Diego, pp 391–440
Dykes RW, Rasmusson DD, Hoeltzell PB (1980) Organization of primary somatosensory cortex in cats. J Neurophysiol 43:1527–1546PubMed
Fabri M, Burton H (1991) Ipsilateral cortical connections of primary somatic sensory cortex in rats. J Comp Neurol 311:405–424PubMed
Felleman DJ, Wall JT, Cusick CG, Kaas JH (1983) The representation of the body surface in S-I of cats. J Neurosci 3:1648–1669PubMedPubMedCentral
Flaherty AW, Graybiel AM (1991) Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. J Neurophysiol 66:1249–1263PubMed
Flaherty AW, Graybiel AM (1993) Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey. J Neurosci 13:1120–1137PubMedPubMedCentral
Flaherty AW, Graybiel AM (1995) Motor and somatosensory corticostriatal projection magnifications in the squirrel monkey. J Neurophysiol 74:2638–2648PubMed
Friend DM, Kravitz AV (2014) Working together: basal ganglia pathways in action selection. Trends Neurosci 37:301–303PubMedPubMedCentral
Gao Z, Davis C, Thomas AM, Economo MN, Abrego AM, Svoboda K, De Zeeuw CI, Li N (2018) A cortico-cerebellar loop for motor planning. Nature 563:113–116PubMedPubMedCentral
Ghosh S, Brinkman C, Porter R (1987) A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J Comp Neurol 259:424–444PubMed
Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23–38
Hamadjida A, Dea M, Deffeyes J, Quessy S, Dancause N (2016) Parallel cortical networks formed by modular organization of primary motor cortex outputs. Curr Biol 26:1737–1743PubMed
Hintiryan H, Foster NN, Bowman I, Bay M, Song MY, Gou L, Yamashita S, Bienkowski MS, Zingg B, Zhu M et al (2016) The mouse cortico-striatal projectome. Nat Neurosci 19:1100–1114PubMedPubMedCentral
Hoffer ZS, Alloway KD (2001) Organization of corticostriatal projections from the vibrissal representations in the primary motor and somatosensory cortical areas of rodents. J Comp Neurol 439:87–103PubMed
Hoffer ZS, Hoover JE, Alloway KD (2003) Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row. J Comp Neurol 466:525–544PubMed
Hoffer ZS, Arantes HB, Roth RL, Alloway KD (2005) Functional circuits mediating sensorimotor integration: quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons. J Comp Neurol 488:82–100PubMed
Hooks BM, Papale AE, Paletzki RF, Feroze MW, Eastwood BS, Couey JJ, Winnubst J, Chandrashekar J, Gerfen CR (2018) Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area. Nat Commun 9:3549PubMedPubMedCentral
Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259:819–821PubMed
Hoover JE, Hoffer ZS, Alloway KD (2003) Projections from primary somatosensory cortex to the neostriatum: the role of somatotopic continuity in corticostriatal convergence. J Neurophysiol 89:1576–1587PubMed
Huerta MF, Pons TP (1990) Primary motor cortex receives input from area 3a in macaques. Brain Res 537:367–371PubMed
Ito S-I, Craig AD (2003) Vagal input to lateral area 3a in cat cortex. J Neurophysiol 90:143–154PubMed
Izraeli R, Porter LL (1995) Vibrissal motor cortex in the rat: connections with the barrel field. Exp Brain Res 104:41–54PubMed
Jackson J, Smith JB, Lee AK (2020) The anatomy and physiology of claustrum-cortex interactions. Ann Rev Neurosci 43:231–247PubMed
Jones SEG, Coulter JD, Hendry SHC (1978) Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291–347PubMed
Kaas JH (2004) Evolution of somatosensory and motor cortex in primates. Anat Rec 281:1148–1156
Khateb M, Schiller J, Schiller Y (2017) Feedforward motor information enhances somatosensory responses and sharpens angular tuning of rat S1 barrel cortex neurons. Elife 6:e21843PubMedPubMedCentral
Kincaid AE, Wilson CJ (1996) Corticostriatal innervation of the patch and matrix in the rat neostriatum. J Comp Neurol 374:578–592PubMed
Klaus A, da Silva JA, Costa RM (2019) What, if, and when to move: basal ganglia circuits and self-paced action initiation. Ann Rev Neurosci 42:459–483PubMed
Kunzle H (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88:195–209PubMed
Kunzle H (1977) Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30:481–492PubMed
Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B (2013) A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci 16:1662–1670PubMedPubMedCentral
Lee CR, Yonk AJ, Wiskerke J, Paradiso KG, Tepper JM, Margolis DJ (2019) Opposing influence of sensory and motor cortical input on striatal circuitry and choice behavior. Curr Biol 29:1313–1323PubMedPubMedCentral
Leergaard TB, Alloway KD, Mutic JJ, Bjaalie JG (2000a) Three- dimensional topography of corticopontine projections from rat barrel cortex: correlations with corticostriatal organization. J Neurosci 20:8474–8484PubMedPubMedCentral
Leergaard TB, Lyngstad KA, Thompson JH, Taeymans S, Vos BP, De Schutter E, Bower JM, Bjaalie JG (2000b) Rat somatosensory cerebro- pontocerebellar pathways: spatial relationships of the somatotopic map of the primary somatosensory cortex are preserved in a three-dimensional clustered pontine map. J Comp Neurol 422:246–266PubMed
Leergaard TB, Alloway KD, Pham TA, Bolstad I, Hoffer Z, Pettersen C, Bjaalie JG (2004) Three-dimensional topography of corticopontine projections from rat sensorimotor cortex: comparisons with corticostriatal projections reveal diverse integrative organization. J Comp Neurol 478:306–322PubMed
Legg CR, Mercier B, Glickstein M (1989) Corticopontine projection in the rat: the distribution of labeled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 286:427–441PubMed
Levesque M, Charara A, Gagnon S, Parent A, Deschenes M (1996) Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res 709:311–315PubMed
Lu SM, Lin RC (1993) Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens Mot Res 10:1–16PubMed
Macchi G, Bentivoglio M, Minciacchi D, Molinari M (1981) The organization of the claustroneocortical projections in the cat studied by means of the HRP retrograde axonal transport. J Comp Neurol 195:681–695PubMed
Mao T, Kusefoglu D, Hooks BM, Huber D, Petreanu L, Svoboda K (2011) Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72:111–123PubMedPubMedCentral
Matyas F, Sreenivasan V, Marbach F, Waconge C, Barsy B, Mateo C, Aronoff R, Petersen CH (2010) Motor control by sensory cortex. Science 330:1240–1243PubMed
Mercier BE, Legg CR, Glickstein M (1990) Basal ganglia and cerebellum receive different somatosensory information in rats. Proc Natl Acad Sci USA 87:4388–4392PubMedPubMedCentral
Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250PubMed
Mori A (1997) Cortico-cortical connections from somatosensory areas to the motor area of the cortex following peripheral nerve lesion in the cat. NeuroReport 8:3723–3726PubMed
Murphy WJ, Pevzner PA, O’Brien SJ (2004) Mammalian phylogenomics comes of age. Trends Genet 20:631–639PubMed
Murthy VN, Fetz EE (1992) Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 89(12):5670–5674PubMedPubMedCentral
Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q et al (2014) A mesoscale connectome of the mouse brain. Nature 508:207–214PubMedPubMedCentral
Pais-Vieira M, Lebedev MA, Wiest MC, Nicolelis MAL (2013) Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination. J Neurosci 33:4076–4093PubMedPubMedCentral
Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 20:91–127PubMed
Pearson RC, Brodal P, Gatter KC, Powell TP (1982) The organization of the connections between the cortex and the claustrum in the monkey. Brain Res 234:435–441PubMed
Proville RD, Spolidoro M, Guyon N, Dugue GP, Selimi F, Isope P, Popa D, Lena C (2014) Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements. Nat Neurosci 17:1233–1239PubMed
Ragsdale CW, Graybiel AM (1981) The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by actetylcholinesterase histochemistry. Brain Res 208:259–266PubMed
Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158–8169PubMedPubMedCentral
Ramnani N (2006) The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7:511–522PubMed
Redgrave P, Prescott TJ, Gurney K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009–1023PubMed
Royce GJ (1982) Laminar origin of cortical neurons which project upon the caudate nucleus: a horseradish peroxidase investigation in the cat. J Comp Neurol 205:8–29PubMed
Schmahmann JD, Pandya DN (1997) The cerebrocerebellar system. Int Rev Neurobiol 41:31–60PubMed
Schwarz C, Mock M (2001) Spatial arrangement of cerebro-pontine terminals. J Comp Neurol 435:418–432PubMed
Schwarz C, Thier P (1995) Modular organization of the pontine nuclei: dendritic fields of identified pontine projection neurons in the rat respect the borders of cortical afferent fields. J Neurosci 15:3475–3489PubMedPubMedCentral
Sherk H (1986) The claustrum and the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex: Sensory-motor areas and aspects of cortical connectivity. Plenum, New York
Smith JB, Alloway KD (2010) Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J Neurosci 30:16832–16844PubMedPubMedCentral
Smith JB, Alloway KD (2013) Rat whisker motor cortex is subdivided into sensory-input and motor-output areas. Front Neural Circuits 7:4PubMedPubMedCentral
Smith JB, Alloway KD (2014) Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front Syst Neurosci 8:93PubMedPubMedCentral
Smith JB, Radhakrishnan H, Alloway KD (2012) Rat claustrum coordinates but does not integrate somatosensory and motor cortical information. J Neurosci 32:8583–8588PubMedPubMedCentral
Smith JB, Alloway KD, Hof PR, Orman R, Reser DH, Watakabe A et al (2019a) The relationship between the claustrum and endopiriform nucleus: a perspective towards consensus on cross-species homology. J Comp Neurol 527:476–499PubMed
Spreafico R, Hayes NL, Rustioni A (1981) Thalamic projections to the primary and secondary somatosensory cortices in cat: Single and double retrograde tracer studies. J Comp Neurol 203:67–90PubMed
Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330:238–271PubMed
Suter BA, Shepherd GMG (2015) Reciprocal interareal connections to corticospinal neurons in mouse M1 and S2. J Neurosci 35:2959–2974PubMedPubMedCentral
Suzuki L, Coulon P, Sabel-Goedknegt RTJH (2012) Organization of cerebral projections to identified cerebellar zones in the posterior cerebellum of the rat. J Neurosci 32:10854–10869PubMedPubMedCentral
Umeda T, Isa T, Nishimura Y (2019) The somatosensory cortex receives information about motor output. Sci Adv 5(7):eaaw5388PubMedPubMedCentral
Vogt BA, Pandya DN (1977) Cortico-cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey. J Comp Neurol 177:179–191
Wiesendanger R, Wiesendanger M (1982a) The corticopontine system in the rat. I. Mapping of corticopontine neurons. J Comp Neurol 208:215–226PubMed
Wiesendanger R, Wiesendanger M (1982b) The corticopontine system in the rat. II. The Projection Pattern. J Comp Neurol 208:227–238PubMed
Wiesendanger R, Wiesendanger M, Ruegg DG (1979) An anatomical investigation of the corticopontine projection in the primate (Macaca fascicularis and Saimiri sciureus)—II. The projection from frontal and parental association areas. Neuroscience 4:747–765PubMed
Zagha E, Casale AE, Sachdev RNS, McGinley MJ, McCormick DA (2013) Motor cortex feedback influences sensory processing by modulating network state. Neuron 79:567–578PubMedPubMedCentral
Metadata
Title
Convergence of forepaw somatosensory and motor cortical projections in the striatum, claustrum, thalamus, and pontine nuclei of cats
Authors
Jared B. Smith
Shubhodeep Chakrabarti
Todd M. Mowery
Kevin D. Alloway
Publication date
01-01-2022
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02405-6

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