Table of Contents
Advances in Neuroscience
Volume 2014, Article ID 862048, 6 pages
http://dx.doi.org/10.1155/2014/862048
Review Article

The Role of Habenula in Motivation and Reward

Department of Neuroscience, Faculty of Medicine, University of Montreal, Montreal QC, Canada H2V 2S9

Received 2 June 2014; Revised 29 July 2014; Accepted 13 August 2014; Published 26 August 2014

Academic Editor: Daniela Schulz

Copyright © 2014 Marc Fakhoury and Sergio Domínguez López. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. J. Meye, S. Lecca, K. Valentinova, and M. Mameli, “Synaptic and cellular profile of neurons in the lateral habenula,” Frontiers in Human Neuroscience, vol. 7, p. 860, 2013. View at Google Scholar
  2. O. Hikosaka, “The habenula: from stress evasion to value-based decision-making,” Nature Reviews Neuroscience, vol. 11, no. 7, pp. 503–513, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Morissette and S. M. Boye, “Electrolytic lesions of the habenula attenuate brain stimulation reward,” Behavioural Brain Research, vol. 187, no. 1, pp. 17–26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. K. H. Andres, M. V. During, and R. W. Veh, “Subnuclear organization of the rat habenular complexes,” The Journal of Comparative Neurology, vol. 407, no. 1, pp. 130–150, 1999. View at Google Scholar
  5. L. Shelton, L. Becerra, and D. Borsook, “Unmasking the mysteries of the habenula in pain and analgesia,” Progress in Neurobiology, vol. 96, no. 2, pp. 208–219, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Lecourtier, H. C. Neijt, and P. H. Kelly, “Habenula lesions cause impaired cognitive performance in rats: implications for schizophrenia,” European Journal of Neuroscience, vol. 19, no. 9, pp. 2551–2560, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Amat, P. D. Sparks, P. Matus-Amat, J. Griggs, L. R. Watkins, and S. F. Maier, “The role of the habenular complex in the elevation of dorsal raphe nucleus serotonin and the changes in the behavioral responses produced by uncontrollable stress,” Brain Research, vol. 917, no. 1, pp. 118–126, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Herkenham and W. J. H. Nauta, “Efferent connections of the habenular nuclei in the rat,” Journal of Comparative Neurology, vol. 187, no. 1, pp. 19–47, 1979. View at Publisher · View at Google Scholar · View at Scopus
  9. K. M. Velasquez, D. L. Molfese, and R. Salas, “The role of the habenula in drug addiction,” Frontiers in Human Neuroscience, vol. 8, article 174, 2014. View at Publisher · View at Google Scholar
  10. D. Wirtschafter, K. E. Asin, and M. R. Pitzer, “Dopamine agonists and stress produce different patterns of Fos-like immunoreactivity in the lateral habenula,” Brain Research, vol. 633, no. 1-2, pp. 21–26, 1994. View at Publisher · View at Google Scholar · View at Scopus
  11. D. M. Gao, D. Huffman, and A. L. Benabid, “Simultaneous recording of spontaneous activities and nociceptive responses from neurons in the Pars compacta of Substantia nigra and in the lateral habenula,” European Journal of Neuroscience, vol. 8, no. 7, pp. 1474–1478, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Baldwin, R. Alanis, and R. Salas, “The role of the Habenula in nicotine addiction,” Journal of Addiction Research & Therapy, vol. S1, article 002, 2001. View at Google Scholar
  13. C. A. Murphy, A. M. DiCamillo, F. Haun, and M. Murray, “Lesion of the habenular efferent pathway produces anxiety and locomotor hyperactivity in rats: a comparison of the effects of neonatal and adult lesions,” Behavioural Brain Research, vol. 81, no. 1-2, pp. 43–52, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Geisler and M. Trimble, “The lateral habenula: no longer neglected,” CNS Spectrums, vol. 13, no. 6, pp. 484–489, 2008. View at Google Scholar · View at Scopus
  15. O. Hikosaka, S. R. Sesack, L. Lecourtier, and P. D. Shepard, “Habenula: crossroad between the basal ganglia and the limbic system,” Journal of Neuroscience, vol. 28, no. 46, pp. 11825–11829, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Iwahori, “A Golgi study on the habenular nucleus of the cat,” Journal of Comparative Neurology, vol. 171, no. 3, pp. 319–344, 1977. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Claudio Cuello, P. C. Emson, G. Paxinos, and T. Jessell, “Substance P containing and cholinergic projections from the habenula,” Brain Research, vol. 149, no. 2, pp. 413–429, 1978. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Brinschwitz, A. Dittgen, V. I. Madai, R. Lommel, S. Geisler, and R. W. Veh, “Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain,” Neuroscience, vol. 168, no. 2, pp. 463–476, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates—The New Coronal Set, Academic Press, 6th edition, 2007.
  20. S. Hong, T. C. Jhou, M. Smith, K. S. Saleem, and O. Hikosaka, “Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates,” The Journal of Neuroscience, vol. 31, no. 32, pp. 11457–11471, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Matsumoto and O. Hikosaka, “Representation of negative motivational value in the primate lateral habenula,” Nature Neuroscience, vol. 12, no. 1, pp. 77–84, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. L. W. Swanson and W. M. Cowan, “The connections of the septal region in the rat,” Journal of Comparative Neurology, vol. 186, no. 4, pp. 621–655, 1979. View at Publisher · View at Google Scholar · View at Scopus
  23. J. H. Fallon and R. Y. Moore, “Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum,” Journal of Comparative Neurology, vol. 180, no. 3, pp. 545–572, 1978. View at Publisher · View at Google Scholar · View at Scopus
  24. R. A. Wise, “Roles for nigrostriatal—not just mesocorticolimbic—dopamine in reward and addiction,” Trends in Neurosciences, vol. 32, no. 10, pp. 517–524, 2009. View at Publisher · View at Google Scholar
  25. S. Ikemoto, “Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory,” Neuroscience & Biobehavioral Reviews, vol. 35, pp. 129–150, 2010. View at Google Scholar
  26. N. Omelchenko, R. Bell, and S. R. Sesack, “Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area,” European Journal of Neuroscience, vol. 30, no. 7, pp. 1239–1250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. J. J. Balcita-Pedicino, N. Omelchenko, R. Bell, and S. R. Sesack, “Sesack inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus,” Journal of Comparative Neurology, vol. 519, pp. 1143–1164, 2011. View at Google Scholar
  28. C. H. Good, H. Wang, Y. H. Chen, C. A. Mejias-Aponte, A. F. Hoffman, and C. R. Lupica, “Dopamine D4 receptor excitation of lateral habenula neurons via multiple cellular mechanisms,” The Journal of Neuroscience, vol. 33, no. 43, pp. 16853–16864, 2013. View at Google Scholar
  29. T. C. Jhou, S. Geisler, M. Marinelli, B. A. Degarmo, and D. S. Zahm, “The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta,” Journal of Comparative Neurology, vol. 513, no. 6, pp. 566–596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Matsumoto and O. Hikosaka, “Lateral habenula as a source of negative reward signals in dopamine neurons,” Nature, vol. 447, no. 7148, pp. 1111–1115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Ellison, “Stimulant-induced psychosis, the dopamine theory of schizophrenia, and the habenula,” Brain Research Reviews, vol. 19, no. 2, pp. 223–239, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Shelton, G. Pendse, N. Maleki et al., “Mapping pain activation and connectivity of the human habenula,” Journal of Neurophysiology, vol. 107, no. 10, pp. 2633–2648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. I. H. Bianco and S. W. Wilson, “The habenular nuclei: A conserved asymmetric relay station in the vertebrate brain,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 364, no. 1519, pp. 1005–1020, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. G. R. Christoph, R. J. Leonzio, and K. S. Wilcox, “Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rabbit,” Journal of Neuroscience, vol. 6, no. 3, pp. 613–619, 1986. View at Google Scholar · View at Scopus
  35. C. Sego, L. Gonτalves, L. Lima, IC. Furigo, J. Donato Jr., and M. Metzger, “Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat,” Journal of Comparative Neurology, vol. 522, no. 7, pp. 1454–1484, 2014. View at Google Scholar
  36. A. L. Benabid and L. Jeaugey, “Cells of the rat lateral habenula respond to high-threshold somatosensory inputs,” Neuroscience Letters, vol. 96, no. 3, pp. 289–294, 1989. View at Publisher · View at Google Scholar · View at Scopus
  37. M. J. Millan, “The induction of pain: an integrative review,” Progress in Neurobiology, vol. 57, no. 1, pp. 1–164, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. W. J. Smith, J. Stewart, and J. G. Pfaus, “Tail pinch induces fos immunoreactivity within several regions of the male rat brain: effects of age,” Physiology and Behavior, vol. 61, no. 5, pp. 717–723, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Lehner, E. Taracha, A. Skórzewska et al., “Sensitivity to pain and c-Fos expression in brain structures in rats,” Neuroscience Letters, vol. 370, no. 1, pp. 74–79, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. P. E. Paulson, J. W. Wiley, and T. J. Morrow, “Concurrent activation of the somatosensory forebrain and deactivation of periaqueductal gray associated with diabetes-induced neuropathic pain,” Experimental Neurology, vol. 208, no. 2, pp. 305–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Welberg, “Psychiatric disorders: reining in the habenula?” Nature Reviews Neuroscience, vol. 14, no. 10, pp. 668–669, 2013. View at Google Scholar
  42. J. Shumake, E. Edwards, and F. Gonzalez-Lima, “Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior,” Brain Research, vol. 963, no. 1-2, pp. 274–281, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. J. B. Savitz, O. Bonne, A. C. Nugent et al., “Habenula volume in post-traumatic stress disorder measured with high-resolution MRI,” Biology of Mood & Anxiety Disorders, vol. 1, no. 1, article 7, 2011. View at Publisher · View at Google Scholar
  44. J. P. Roiser, J. Levy, S. J. Fromm et al., “The effects of tryptophan depletion on neural responses to emotional words in remitted depression,” Biological Psychiatry, vol. 66, no. 5, pp. 441–450, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. J. B. Savitz, A. C. Nugent, W. Bogers et al., “Habenula volume in bipolar disorder and major depressive disorder: a high-resolution magnetic resonance imaging study,” Biological Psychiatry, vol. 69, no. 4, pp. 336–343, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Sartorius, K. L. Kiening, P. Kirsch et al., “Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient,” Biological Psychiatry, vol. 67, no. 2, pp. e9–e11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Meng, Y. Wang, M. Huang, W. Lin, S. Wang, and B. Zhang, “Chronic deep brain stimulation of the lateral habenula nucleus in a rat model of depression,” Brain Research, vol. 1422, pp. 32–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. R. B. Whitelaw, A. Markou, T. W. Robbins, and B. J. Everitt, “Excitotoxic lesions of the basolateral amygdala impair the acquisition of cocaine-seeking behaviour under a second-order schedule of reinforcememt,” Psychopharmacology, vol. 127, no. 3, pp. 213–224, 1996. View at Publisher · View at Google Scholar · View at Scopus
  49. E. D. Kirby, K. Jensen, K. A. Goosens, and D. Kaufer, “Stereotaxic surgery for excitotoxic lesion of specific brain areas in the adult rat,” Journal of Visualized Experiment, no. 65, Article ID e4079, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Sourani, R. Eitan, N. Gordon, and G. Goelman, “The habenula couples the dopaminergic and the serotonergic systems: application to depression in Parkinson's disease,” European Journal of Neuroscience, vol. 36, no. 6, pp. 2822–2829, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Carey, D. Danna Paul, and I. Greg, “The habenula governs the attribution of incentive salience to reward predictive cues,” Frontiers in Human Neuroscience, vol. 7, article 781, 2013. View at Google Scholar
  52. R. A. Rescorla and R. L. Solomon, “Two-process learning theory: relationships between Pavlovian conditioning and instrumental learning,” Psychological Review, vol. 74, no. 3, pp. 151–182, 1967. View at Publisher · View at Google Scholar · View at Scopus