Advertisement

Brain Structure and Function

, Volume 223, Issue 1, pp 535–543 | Cite as

Opposing collicular influences on the parafascicular (Pf) and posteromedial (POm) thalamic nuclei: relationship to POm-induced inhibition in the substantia nigra pars reticulata (SNR)

  • Glenn D. R. Watson
  • Kevin D. AllowayEmail author
Short Communication

Abstract

The superior colliculus activates the zona incerta (ZI), which sends GABAergic projections to the posteromedial (POm) thalamic nucleus. Consistent with this circuit, we previously showed that stimulation of the superior colliculus activates ZI and causes inhibition of neuronal activity in POm (Watson et al., J Neurosci 35:9463–9476, 2015). Other studies, however, have shown that collicular stimulation activates the intralaminar nuclei of the thalamus. The present study extends these reports by showing that unilateral collicular stimulation causes bilateral activation of Pf that is concomitant with bilateral inhibition of POm. The opposing influences of the superior colliculus on Pf and POm are significant, because both these thalamic nuclei innervate the striatum, which is involved in behavioral selection. In view of data indicating that thalamostriatal projections from Pf and other intralaminar nuclei increase the sensitivity of the indirect pathway to corticostriatal inputs (Ding et al., Neuron 67:294–307, 2010), we tested whether POm stimulation might exert an opposing influence on the basal ganglia circuitry. Consistent with POm projections to the dorsolateral striatum (DLS), which is necessary for the expression of sensorimotor habits, we found that POm stimulation activates DLS and causes inhibition of neuronal activity in the lateral part of the substantia nigra pars reticulata, which is a major target of DLS and the direct pathway. These findings are discussed with respect to clinical reports indicating that deep brain stimulation in ZI is effective in reducing the symptoms of Parkinson’s disease.

Keywords

Superior colliculus Optogenetic stimulation Thalamostriatal Dorsolateral striatum Basal ganglia 

Notes

Acknowledgements

This work was supported by the Grace Woodward Foundation and Pennsylvania State University. The authors thank Dr. Jared B. Smith for constructive comments on earlier versions of this paper, and we acknowledge use of the Microscopy Core in The Huck Institutes of the Life Sciences at Penn State University.

References

  1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375CrossRefPubMedGoogle Scholar
  2. Alloway KD, Smith JB, Watson GDR (2014) Thalamostriatal projections from the medial posterior and parafascicular nuclei have distinct topographic and physiologic properties. J Neurophysiol 111:36–50CrossRefPubMedGoogle Scholar
  3. Alloway KD, Smith JB, Mowery TM, Watson GDR (2017) Sensory processing in the dorsolateral striatum: the contribution of thalamostriatal pathways. Front Syst Neurosci 11:53. doi: 10.3389/fnsys.2017.00053 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bartho P, Freund TF, Acsady L (2002) Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci 16:999–1014CrossRefPubMedGoogle Scholar
  5. Blomstedt P, Fytagoridis A, Astrom M, Linder J, Forsgren L (2012) Unilateral caudal zona incerta deep brain stimulation for Parkinsonian tremor. Parkinsonism Relat Disord 18:1062–1066CrossRefPubMedGoogle Scholar
  6. Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation, 2nd edn. Wiley, HobokenCrossRefGoogle Scholar
  7. Caire F, Ranoux D, Guehl D, Burband Cuny E (2013) A systematic review of studies on anatomical position of electrode contacts for chronic subthalamic stimulation in Parkinson’s disease. Acta Neurochir 155:1647–1654CrossRefPubMedGoogle Scholar
  8. Carvell GE, Simons DJ (1987) Thalamic and corticocortical connections of the second somatosensory area of the mouse. J Comp Neurol 265:409–427CrossRefPubMedGoogle Scholar
  9. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285CrossRefPubMedGoogle Scholar
  10. Deschênes M, Bourassa J, Parent A (1995) Two different types of thalamic fibers innervate the rat striatum. Brain Res 701:288–292CrossRefPubMedGoogle Scholar
  11. Deschênes M, Bourassa J, Doan VD, Parent A (1996) A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur J Neurosci 8:329–343CrossRefPubMedGoogle Scholar
  12. Ding JB, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294–307CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dray A, Gonye TJ, Oakley NR (1976) Caudate stimulation and substantia nigra activity in the rat. J Physiol 259:825–849CrossRefPubMedPubMedCentralGoogle Scholar
  14. Freeze BS, Kravitz AV, Hammack Berke JD, Kreitzer AC (2013) Control of basal ganglia output by direct and indirect pathway projections neurons. J Neurosci 33:18531–18539CrossRefPubMedPubMedCentralGoogle Scholar
  15. Friedberg MH, Lee SM, Ebner FF (1999) Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 81:2243–2252CrossRefPubMedGoogle Scholar
  16. Gangaroosa G, Espallergues J, Mailly P, De Buindel D, Kerchove d’Exaerde A, Herve D, Girault JA, Valjent E, Krieger P (2013) Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum. Front Neural Circuits 7:124Google Scholar
  17. Garcia-Garcia D, Guridi J, Toledo JB, Alegre M, Obeso JA, Rodriguez-Oroz MC (2016) Stimulation sites in the subthalamic nucleus and clinical improvement in Parkinson’s disease: a new approach for active contact localization. J Neurosurg 125:1068–1079CrossRefPubMedGoogle Scholar
  18. Gerfen CR (2004) Basal ganglia. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, New York, pp 455–508CrossRefGoogle Scholar
  19. Groenewegen HJ, Berendse HW (1994) The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci 17:52–57CrossRefPubMedGoogle Scholar
  20. Grunwerg BS, Krauthamer GM (1992) Sensory responses of intralaminar thalamic neurons activated by the superior colliculus. Exp Brain Res 88:541–550CrossRefPubMedGoogle Scholar
  21. Hikosaka O, Sakamoto M, Miyashita N (1993) Effects of caudate nucleus stimulation on substantia nigra cell activity in the monkey. Exp Brain Res 95:457–472CrossRefPubMedGoogle Scholar
  22. Krauthamer GM, Krol JG, Grunwerg BS (1992) Effect of superior colliculus lesions on sensory unit responses in the intralaminar thalamus of the rat. Brain Res 576:277–286CrossRefPubMedGoogle Scholar
  23. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622–626CrossRefPubMedPubMedCentralGoogle Scholar
  24. Krout KE, Loewy AD, Westby GWM, Redgrave P (2001) Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 431:198–216CrossRefPubMedGoogle Scholar
  25. Lacey CJ, Bolam JP, Magill PJ (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27:4374–4384CrossRefPubMedGoogle Scholar
  26. Lukins TR, Tisch S, Jonker B (2014) The latest evidence on target selection in deep brain stimulation for Parkinson’s disease. J Clin Neurosci 21:22–27CrossRefPubMedGoogle Scholar
  27. May PJ (2006) The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151:321–378CrossRefPubMedGoogle Scholar
  28. Mitrofanis J (2005) Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta. Neuroscience 130:1–15CrossRefPubMedGoogle Scholar
  29. Mowery TM, Harold J, Alloway KD (2011) Repeated whisker stimulation evokes invariant neuronal responses in the dorsolateral striatum of anesthetized rats: a potential correlate of sensorimotor habits. J Neurophysiol 105:2225–2238CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ohno S, Kuramoto E, Furuta T, Hioka H, Tanaka YR, 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 22:2840–2857CrossRefPubMedGoogle Scholar
  31. Power BD, Mitrofanis J (2001) Zona incerta: substrate for contralateral interconnectivity in the thalamus of rats. J Comp Neurol 451:33–44CrossRefGoogle Scholar
  32. Reiner A, Jiao Y, Del Mar N, Laverghetta AV, Lei WL (2003) Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457:420–440CrossRefPubMedGoogle Scholar
  33. Sippy T, Lapray D, Crochet S, Petersen CCH (2015) Celltype-specific sensorimotor processing in striatal projection neurons during goal-directed behavior. Neuron 88:298–305CrossRefPubMedPubMedCentralGoogle Scholar
  34. Smith Y, Raju DV, Pare JF, Sidibe M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27:520–527CrossRefPubMedGoogle Scholar
  35. Smith JB, Mowery TM, Alloway KD (2012) Thalamic POm projections to the dorsolateral striatum of rats: potential pathway for mediating stimulus-response associations for sensorimotor habits. J Neurophysiol 108:160–174CrossRefPubMedPubMedCentralGoogle Scholar
  36. Thorn CA, Graybiel AM (2010) Pausing to regroup: thalamic gating of cortico-basal ganglia networks. Neuron 67:175–178CrossRefPubMedGoogle Scholar
  37. Tulloch IF, Arbuthnott GW, Wright AK (1978) Topographical organization of the striatonigral pathway revealed by anterograde and retrograde neuroanatomical tracing methods. J Anat 127:425–441PubMedPubMedCentralGoogle Scholar
  38. Watson GDR, Smith JB, Alloway KD (2015) The zona incerta regulates communication between the superior colliculus and the posteromedial thalamus: implications for thalamic interactions with the dorsolateral striatum. J Neurosci 35:9463–9476CrossRefPubMedPubMedCentralGoogle Scholar
  39. Yin HH, Knowlton BJ, Balleine BW (2004) Lesions of the dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19:181–189CrossRefPubMedGoogle Scholar
  40. Yin HH, Knowlton BJ, Balleine BW (2006) Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 166:189–196CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Neural and Behavioral SciencesPennsylvania State University College of MedicineHersheyUSA
  2. 2.Center for Neural Engineering, Millennium Science ComplexPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations