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On the Relationships Between the Pedunculopontine Tegmental Nucleus, Corticostriatal Architecture, and the Medial Reticular Formation

  • David I. G. Wilson
  • Duncan A. A. MacLaren
  • Philip Winn
Conference paper
Part of the Advances in Behavioral Biology book series (ABBI, volume 58)

Abstract

Recent studies have established that the pedunculopontine tegmental nucleus (PPTg) is integrated into corticostriatal looped architecture through connections that include established basal ganglia output nuclei (pallidum, subthalamus and substantia nigra pars reticulata), thalamus and midbrain dopamine (DA) containing neurons in both the ventral tegmental area (VTA) and substantia nigra pars compacta (SNC). It is becoming apparent that the PPTg can be functionally dissociated internally. A simple dissociation is between posterior and anterior PPTg. The posterior PPTg contains a large proportion of cholinergic neurons, has polymodal sensory input that triggers very fast neuronal activity and projects preferentially to the VTA. In contrast, the anterior PPTg contains fewer cholinergic neurons, receives outflow from both corticostriatal systems and the extended amygdala and projects to the SNC. We suggest that this organization maps on to the spiral corticostriatal architecture such that the posterior PPTg interacts with ventromedial striatal systems (a proposed function of which is to integrate incentive salient stimuli to shape flexible goal-directed actions), whereas the anterior PPTg interacts with dorsolateral striatal circuits (which are thought to mediate the learning and execution of stimulus–response associations and the formation of habits). By these interactions, the PPTg en masse contributes to high-order decision making processes that shape action selection. In addition to this we also suggest that the PPTg integrates with medial reticular formation systems that operate as an immediate low-level action selection mechanism. We hypothesize that the PPTg has a pivotal position, bridging between higher order action selection mechanisms dealing with flexible learning of novel action patterns and lower level action selection processes that permit very fast responding to imperative stimuli.

Keywords

Basal Ganglion Conditioned Stimulus Ventral Tegmental Area Ventral Striatum Dorsal Striatum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

David Wilson and Duncan MacLaren are supported by Wellcome Trust project grant 081128 to PW. We wish to extend our thanks to the editors for their patience and kindness in allowing us extra time in which to complete this essay.

References

  1. Ainge JA, Jenkins TA and Winn P (2004) Induction of c-fos in specific thalamic nuclei following stimulation of the pedunculopontine tegmental nucleus. Eur J Neurosci 20: 1827–1837.CrossRefPubMedGoogle Scholar
  2. Alderson HL, Parkinson JA, Robbins TW and Everitt BJ (2001) The effects of excitotoxic lesions of the nucleus accumbens core or shell regions on intravenous heroin self-administration in rats. Psychopharmacology (Berl) 153: 455–463.CrossRefGoogle Scholar
  3. Alderson HL, Latimer MP, Blaha CD, Phillips AG and Winn P (2004) An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience 125: 349–358.CrossRefPubMedGoogle Scholar
  4. Alderson HL, Latimer MP and Winn P (2006) Intravenous self-administration of nicotine is altered by lesions of the posterior, but not anterior, pedunculopontine tegmental nucleus. Eur J Neurosci 23: 2169–2175.CrossRefPubMedGoogle Scholar
  5. Alderson HL, Latimer MP and Winn P (2008) A functional dissociation of the anterior and posterior pedunculopontine tegmental nucleus: Excitotoxic lesions have differential effects on locomotion and the response to nicotine. Brain Struct Funct 213: 247–253.CrossRefPubMedGoogle Scholar
  6. Atallah HE, Lopez-Paniagua D, Rudy JW and O’Reilly RC (2007) Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nat Neurosci 10:126–131.CrossRefPubMedGoogle Scholar
  7. Balleine B and Killcross S (1994) Effects of ibotenic acid lesions of the nucleus accumbens on instrumental action. Behav Brain Res 65: 181–193.CrossRefPubMedGoogle Scholar
  8. Belin D and Everitt BJ (2008) Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57: 432–441.CrossRefPubMedGoogle Scholar
  9. Berridge KC (2003) Pleasures of the brain. Brain Cogn 52: 106–128.CrossRefPubMedGoogle Scholar
  10. Berridge KC and Robinson TE (1998) What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28: 309–369.CrossRefPubMedGoogle Scholar
  11. Bowman EM, Aigner TG and Richmond BJ (1996) Neural signals in the monkey ventral striatum related to motivation for juice and cocaine rewards. J Neurophysiol 75: 1061–1073.PubMedGoogle Scholar
  12. Cardinal RN and Cheung TH (2005) Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat. BMC Neurosci 6: 9.CrossRefPubMedGoogle Scholar
  13. Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW and Everitt, BJ (2001) Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292: 2499–2501.CrossRefPubMedGoogle Scholar
  14. Clarke NP, Bevan MD, Cozzari C, Hartman BK and Bolam JP (1997) Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and subthalamic nucleus of the rat. Neuroscience 81: 371–385.CrossRefPubMedGoogle Scholar
  15. Corbit LH, Muir JL and Balleine BW (2001) The role of the nucleus accumbens in instrumental conditioning: Evidence of a functional dissociation between accumbens core and shell. J Neurosci 21: 3251–3260.PubMedGoogle Scholar
  16. Corrigall WA, Coen KM and Adamson KL (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653: 279–284.CrossRefGoogle Scholar
  17. de Borchgrave R, Rawlins JN, Dickinson A and Balleine BW (2002) Effects of cytotoxic nucleus accumbens lesions on instrumental conditioning in rats. Exp Brain Res 144: 50–68.CrossRefPubMedGoogle Scholar
  18. Di Ciano P, Robbins TW and Everitt BJ (2008) Differential effects of nucleus accumbens core, shell, or dorsal striatal inactivations on the persistence, reacquisition, or reinstatement of responding for a drug-paired conditioned reinforcer. Neuropsychopharmacology 33: 1413–1425.CrossRefPubMedGoogle Scholar
  19. Dickinson A (1985) Actions and habits: The development of behavioural autonomy. Philos Trans R Soc Lond B Biol Sci 308: 67–78.CrossRefGoogle Scholar
  20. Dickinson A, Balleine BW, Watt A, Gonzales F and Boakes RA (1995) Overtraining and the motivational control of instrumental action. Anim Learn Behav 22: 197–206.Google Scholar
  21. Dormont JF, Conde H and Farin D (1998) The role of the pedunculopontine tegmental nucleus in relation to conditioned motor performance in the cat. I. Context-dependent and reinforcement-related single unit activity. Exp Brain Res 121: 401–410.CrossRefPubMedGoogle Scholar
  22. Erro E, Lanciego JL and Gimenez-Amaya JM (1999) Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: A neuroanatomical tract-tracing study in the rat. Exp Brain Res 127: 162–170.CrossRefPubMedGoogle Scholar
  23. Evenden JL and Carli M (1985) The effects of 6-hydroxydopamine lesions of the nucleus accumbens and caudate nucleus of rats on feeding in a novel environment. Behav Brain Res 15: 63–70.CrossRefPubMedGoogle Scholar
  24. Everitt BJ and Robbins TW (2005) Neural systems of reinforcement for drug addiction: From actions to habits to compulsion. Nat Neurosci 8: 1481–1489.CrossRefPubMedGoogle Scholar
  25. Faure A, Haberland U, Conde F and El Massioui N (2005) Lesion to the nigrostriatal dopamine system disrupts stimulus–response habit formation. J Neurosci 25: 2771–2780.CrossRefPubMedGoogle Scholar
  26. Gillies AJ and Willshaw DJ (1998) A massively connected subthalamic nucleus leads to the generation of widespread pulses. Proc R Soc Lond B 265: 2101–2109.CrossRefGoogle Scholar
  27. Grace AA, Floresco SB, Goto Y and Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30: 220–227.CrossRefPubMedGoogle Scholar
  28. Grillner S, Hellgren J, Menard A, Saitoh K and Wikstrom MA (2005) Mechanisms for selection of basic motor programs – roles for the striatum and pallidum. Trends Neurosci 28: 364–370.CrossRefPubMedGoogle Scholar
  29. Haber SN (2003) The primate basal ganglia: Parallel and integrative networks. J Chem Neuroanat 26: 317–330.CrossRefPubMedGoogle Scholar
  30. Hall J, Parkinson JA, Connor TM, Dickinson A and Everitt BJ (2001) Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating pavlovian influences on instrumental behaviour. Eur J Neurosci 13: 1984–1992.CrossRefPubMedGoogle Scholar
  31. Hernandez PJ, Sadeghian K and Kelley AE (2002) Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat Neurosci 5: 1327–1331.CrossRefPubMedGoogle Scholar
  32. Hikosaka O (1998) Neural systems for control of voluntary action – a hypothesis. Adv Biophys 35: 81–102.CrossRefPubMedGoogle Scholar
  33. Hikosaka O (2007) GABAergic output of the basal ganglia. Prog Brain Res 160: 209–226.CrossRefPubMedGoogle Scholar
  34. Humphries MD, Gurney K and Prescott TJ (2007) Is there a brainstem substrate for action selection? Philos Trans R Soc Lond B Biol Sci 362: 1627–1639.CrossRefPubMedGoogle Scholar
  35. Hutcheson DM, Parkinson JA, Robbins TW and Everitt BJ (2001) The effects of nucleus accumbens core and shell lesions on intravenous heroin self-administration and the acquisition of drug-seeking behaviour under a second-order schedule of heroin reinforcement. Psychopharmacology 153: 464–472.CrossRefPubMedGoogle Scholar
  36. Ikemoto S (2007) Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex. Brain Res Rev 56: 27–78.CrossRefPubMedGoogle Scholar
  37. Ito R, Robbins TW and Everitt BJ (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7: 389–397.CrossRefPubMedGoogle Scholar
  38. Joel D and Weiner I (2000) The connections of the dopaminergic system with the striatum in rats and primates: An analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96: 451–474.CrossRefPubMedGoogle Scholar
  39. Keating GL and Winn P (2002) Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay. Neuroscience 112: 687–696.CrossRefPubMedGoogle Scholar
  40. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59: 107–128.CrossRefPubMedGoogle Scholar
  41. Koch M, Kungel M and Herbert H (1993) Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp Brain Res 97: 71–82.CrossRefPubMedGoogle Scholar
  42. Lodge DJ and Grace AA (2006) The hippocampus modulates dopamine neuron responsivity by regulating the intensity of phasic neuron activation. Neuropsychopharmacology 31: 1356–1361.CrossRefPubMedGoogle Scholar
  43. Lyon M and Robbins TW (1975) The action of central nervous system stimulant drugs: A general theory concerning amphetamine effects In: Essman W, Valzelli L (eds) Current developments in psychopharmacology. Spectrum, New York, NY.Google Scholar
  44. Maskos U (2008) The cholinergic mesopontine tegmentum is a relatively neglected nicotinic master modulator of the dopaminergic system: Relevance to drugs of abuse and pathology. Br J Pharmacol 153(Suppl 1): S438–S445.PubMedGoogle Scholar
  45. McHaffie JG, Stanford TR, Stein BE, Coizet V and Redgrave P (2005) Subcortical loops through the basal ganglia. Trends Neurosci 28: 401–407.CrossRefPubMedGoogle Scholar
  46. Mena-Segovia J, Bolam JP and Magill PJ (2004) Pedunculopontine nucleus and basal ganglia: Distant relatives or part of the same family? Trends Neurosci 27: 585–588.CrossRefPubMedGoogle Scholar
  47. Mena-Segovia J, Winn P and Bolam JP (2008) Cholinergic modulation of midbrain dopaminergic systems. Brain Res Rev 58: 265–271.CrossRefPubMedGoogle Scholar
  48. Mesulam MM, Mufson EJ, Wainer BH and Levey AI (1983) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6). Neuroscience 10: 1185–1201.CrossRefPubMedGoogle Scholar
  49. Mink JW (1996) The basal ganglia: Focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381–425.CrossRefPubMedGoogle Scholar
  50. Nelson A, Killcross S (2006) Amphetamine exposure enhances habit formation. J Neurosci 26: 3805–3812.CrossRefPubMedGoogle Scholar
  51. Oakman SA, Faris PL, Kerr PE, Cozzari C and Hartman BK (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 15: 5859–5869.PubMedGoogle Scholar
  52. Oakman SA, Faris PL, Cozzari C and Hartman BK (1999) Characterization of the extent of ponto-mesencephalic cholinergic neurons’ projections to the thalamus: Comparison with projections to midbrain dopaminergic groups. Neuroscience 94: 529–547.CrossRefPubMedGoogle Scholar
  53. Packard MG and McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65: 65–72.CrossRefPubMedGoogle Scholar
  54. Pahapill PA and Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123: 1767–1783.CrossRefPubMedGoogle Scholar
  55. Pan WX and Hyland BI (2005) Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J Neurosci 25: 4725–4732.CrossRefPubMedGoogle Scholar
  56. Parent A and Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20: 91–127.CrossRefPubMedGoogle Scholar
  57. Plaha P and Gill SS (2005) Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. Neuroreport 16: 1883–1887.CrossRefPubMedGoogle Scholar
  58. Prescott TJ, Redgrave P and Gurney K (1999) Layered control architectures in robots and vertebrates. Adapt Behav 7: 99–127.CrossRefGoogle Scholar
  59. Reading PJ, Dunnett SB and Robbins TW (1991) Dissociable roles of the ventral, medial and lateral striatum on the acquisition and performance of a complex visual stimulus-response habit. Behav Brain Res 45: 147–161.CrossRefPubMedGoogle Scholar
  60. Redgrave P, Gurney K (2006) The short-latency dopamine signal: A role in discovering novel actions? Nat Rev Neurosci 7: 967–975.CrossRefPubMedGoogle Scholar
  61. Redgrave P, Prescott TJ, Gurney K (1999a) The basal ganglia: A vertebrate solution to the selection problem? Neuroscience 89: 1009–1023.CrossRefPubMedGoogle Scholar
  62. Redgrave P, Prescott TJ and Gurney K (1999b) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22: 146–151.CrossRefPubMedGoogle Scholar
  63. Robbins TW and Koob GF (1980) Selective disruption of displacement behaviour by lesions of the mesolimbic dopamine system. Nature 285: 409–412.CrossRefPubMedGoogle Scholar
  64. Salamone JD, Correa M, Mingote S and Weber SM (2003) Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: Implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 305: 1–8.CrossRefPubMedGoogle Scholar
  65. Schoenbaum G, Roesch MR and Stalnaker TA (2006) Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci 29: 116–124.CrossRefPubMedGoogle Scholar
  66. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1–27.PubMedGoogle Scholar
  67. Shidara M, Aigner TG and Richmond BJ (1998) Neuronal signals in the monkey ventral striatum related to progress through a predictable series of trials. J Neurosci 18: 2613–2625.PubMedGoogle Scholar
  68. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E and Mazzone P (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain 130: 1596–1607.CrossRefPubMedGoogle Scholar
  69. Stewart RD and Dommett EJ (2006) Subcortical control of dopamine neurons: The good, the bad and the unexpected. Brain Res Bull 71: 1–3.CrossRefPubMedGoogle Scholar
  70. Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K and Sakamoto T (2003) Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: A new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 119: 293–308.CrossRefPubMedGoogle Scholar
  71. Tang C, Pawlak AP, Prokopenko V and West MO (2007) Changes in activity of the striatum during formation of a motor habit. Eur J Neurosci 25: 1212–1227.CrossRefPubMedGoogle Scholar
  72. Taylor CL, Kozak R, Latimer MP and Winn P (2004) Effects of changing reward on performance of the delayed spatial win-shift radial maze task in pedunculopontine tegmental nucleus lesioned rats. Behav Brain Res 153: 431–438.CrossRefPubMedGoogle Scholar
  73. Tobler PN, Fiorillo CD and Schultz W (2005) Adaptive coding of reward value by dopamine neurons. Science 307: 1642–1645.CrossRefPubMedGoogle Scholar
  74. Voorn P, Vanderschuren LJ, Groenewegen HJ, Robbins TW and Pennartz CM (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27: 468–474.CrossRefPubMedGoogle Scholar
  75. Walker SC and Winn P (2007) An assessment of the contributions of the pedunculopontine tegmental and cuneiform nuclei to anxiety and neophobia. Neuroscience 150: 273–290.CrossRefPubMedGoogle Scholar
  76. Wickens JR, Horvitz JC, Costa RM and Killcross S (2007) Dopaminergic mechanisms in actions and habits. J Neurosci 27: 8181–8183.CrossRefPubMedGoogle Scholar
  77. Wilson DI and Bowman EM (2004) Nucleus accumbens neurons in the rat exhibit differential activity to conditioned reinforcers and primary reinforcers within a second-order schedule of saccharin reinforcement. Eur J Neurosci 20: 2777–2788.CrossRefPubMedGoogle Scholar
  78. Wilson DI and Bowman EM (2005) Rat nucleus accumbens neurons predominantly respond to the outcome-related properties of conditioned stimuli rather than their behavioral-switching properties. J Neurophysiol 94: 49–61.CrossRefPubMedGoogle Scholar
  79. Winn P (2006) How best to consider the structure and function of the pedunculopontine tegmental nucleus: Evidence from animal studies. J Neurol Sci 248: 234–250.CrossRefPubMedGoogle Scholar
  80. Winn P, Brown VJ and Inglis WL (1997) On the relationships between the striatum and the pedunculopontine tegmental nucleus. Crit Rev Neurobiol 11: 241–261.PubMedGoogle Scholar
  81. Yin HH and Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7: 464–476.CrossRefPubMedGoogle Scholar
  82. Yin HH, Knowlton BJ and Balleine BW (2004) Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19: 181–189.CrossRefPubMedGoogle Scholar
  83. Zahm DS, Williams EA, Latimer MP and Winn P (2001) Ventral mesopontine projections of the caudomedial shell of the nucleus accumbens and extended amygdala in the rat: Double dissociation by organization and development. J Comp Neurol 436: 111–125.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • David I. G. Wilson
    • 1
  • Duncan A. A. MacLaren
    • 1
  • Philip Winn
    • 1
  1. 1.School of PsychologyUniversity of St. Andrews, St. Mary’s QuadScotlandUK

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