Advertisement

Brain Structure and Function

, Volume 222, Issue 4, pp 1971–1988 | Cite as

Abundant collateralization of temporal lobe projections to the accumbens, bed nucleus of stria terminalis, central amygdala and lateral septum

  • Rhett A. Reichard
  • Suriya Subramanian
  • Mikiyas T. Desta
  • Tej Sura
  • Mary L. Becker
  • Comeron W. Ghobadi
  • Kenneth P. Parsley
  • Daniel S. Zahm
Original Article

Abstract

Behavioral flexibility is subserved in part by outputs from the cerebral cortex to telencephalic subcortical structures. In our earlier evaluation of the organization of the cortical–subcortical output system (Reynolds and Zahm, J Neurosci 25:11757–11767, 2005), retrograde double-labeling was evaluated in the prefrontal cortex following tracer injections into pairs of the following subcortical telencephalic structures: caudate–putamen, core and shell of the accumbens (Acb), bed nucleus of stria terminalis (BST) and central nucleus of the amygdala (CeA). The present study was done to assess patterns of retrograde labeling in the temporal lobe after similar paired tracer injections into most of the same telencephalic structures plus the lateral septum (LS). In contrast to the modest double-labeling observed in the prefrontal cortex in the previous study, up to 60–80 % of neurons in the basal and accessory basal amygdaloid nuclei and amygdalopiriform transition area exhibited double-labeling in the present study. The most abundant double-labeling was generated by paired injections into structures affiliated with the extended amygdala, including the CeA, BST and Acb shell. Injections pairing the Acb core with the BST or CeA produced significantly fewer double-labeled neurons. The ventral subiculum exhibited modest amounts of double-labeling associated with paired injections into the Acb, BST, CeA and LS. The results raise the issue of how an extraordinarily collateralized output from the temporal lobe may contribute to behavioral flexibility.

Keywords

Dopamine Motivation Emotion Locomotion Motor Movement 

Abbreviations

ABA

Accessory basal nucleus of the amygdala

ABC

Avidin–biotin–peroxidase complex

Acb

Nucleus accumbens

AcbC

Acb core

AcbS

Acb shell

AHip

Amygdalohippocampal transition area

APir

Amygdalopiriform transition area

BA

Basal nucleus of the amygdala

BST

Bed nucleus of the stria terminalis

CeA

Central nucleus of the amygdala

CPu

Caudate–putamen

Ctβ

Cholera toxin, β subunit

DAB

Diaminobenzidine

FG

FluoroGold

IC

Insular cortex

LS

Lateral septum

mPfC

Medial prefrontal cortex

SPB

Sorenson’s phosphate buffer

VSub

Ventral subiculum

Notes

Acknowledgments

Grant support: USPHS NIH NS-23805.

References

  1. Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985:185–205PubMedCrossRefGoogle Scholar
  2. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1–39PubMedCrossRefGoogle Scholar
  3. Altier N, Stewart J (1998) Dopamine receptor antagonists in the nucleus accumbens attenuate analgesia induced by ventral tegmental area substance P or morphine and by nucleus accumbens amphetamine. J Pharmacol Exp Ther 285:208–215PubMedGoogle Scholar
  4. Altier N, Stewart J (1999) The role of dopamine in the nucleus accumbens in analgesia. Life Sci 65:2269–2287PubMedCrossRefGoogle Scholar
  5. Amorapanth P, LeDoux JE, Nader K (2000) Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 3:74–79PubMedCrossRefGoogle Scholar
  6. Aquili L, Liu AW, Shindou M, Shindou T, Wickens JR (2014) Behavioral flexibility is increased by optogenetic inhibition of neurons in the nucleus accumbens shell during specific time segments. Learn Mem (Cold Spring Harbor, NY) 21:223–231CrossRefGoogle Scholar
  7. Bard P (1928) A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am J Physiol 84:490–515Google Scholar
  8. Bard P, Macht MB (1958) The behaviour of chronically decerebrate cats. In: Wolstenholme GEW, O’Connor CM (eds) Ciba Foundation symposium on the neurological basis of behavior. J & A Churchill, LTD, London, pp 55–75Google Scholar
  9. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 99:11435–11440PubMedPubMedCentralCrossRefGoogle Scholar
  10. Barrot M, Wallace DL, Bolanos CA, Graham DL, Perrotti LI, Neve RL, Chambliss H, Yin JC, Nestler EJ (2005) Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci USA 102:8357–8362PubMedPubMedCentralCrossRefGoogle Scholar
  11. Berendse HW, Galis-de Graaf Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316:314–347PubMedCrossRefGoogle Scholar
  12. Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacol 191:391–431CrossRefGoogle Scholar
  13. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28:309–369PubMedCrossRefGoogle Scholar
  14. Berridge KC, Robinson TE, Aldridge JW (2009) Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr Opin Pharmacol 9:65–73PubMedPubMedCentralCrossRefGoogle Scholar
  15. Block AE, Dhanji H, Thompson-Tardif SF, Floresco SB (2007) Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb Cortex (New York, NY: 1991) 17:1625–1636Google Scholar
  16. Boulougouris V, Dalley JW, Robbins TW (2007) Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 179:219–228PubMedCrossRefGoogle Scholar
  17. Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255–278PubMedCrossRefGoogle Scholar
  18. Calderazzo L, Cavalheiro EA, Macchi G, Molinari M, Bentivoglio M (1996) Branched connections to the septum and to the entorhinal cortex from the hippocampus, amygdala, and diencephalon in the rat. Brain Res Bull 40:245–251PubMedCrossRefGoogle Scholar
  19. Campeau S, Davis M (1995) Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15:2301–2311PubMedGoogle Scholar
  20. Cannon WB, Britton SW (1927) Pseudoaffective medulloadrenal secretion. Am J Physiol 79:4333–4465Google Scholar
  21. Cannon CM, Palmiter RD (2003) Reward without dopamine. J Neurosci 23:10827–10831PubMedGoogle Scholar
  22. Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324:180–194PubMedCrossRefGoogle Scholar
  23. Carlezon WA Jr, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science (New York, NY) 282:2272–2275CrossRefGoogle Scholar
  24. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436–445PubMedCrossRefGoogle Scholar
  25. Carlssen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380CrossRefGoogle Scholar
  26. Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641PubMedCrossRefGoogle Scholar
  27. Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179–207PubMedCrossRefGoogle Scholar
  28. Cassell MD (1998) The amygdala: myth or monolith? Trends Neurosci 21:200–201PubMedCrossRefGoogle Scholar
  29. Cassell MD, Freedman LJ, Shi C (1999) The intrinsic organization of the central extended amygdala. Ann N Y Acad Sci 877:217–241PubMedCrossRefGoogle Scholar
  30. Chen S, Aston-Jones G (1995) Evidence that cholera toxin B subunit (CTb) can be avidly taken up and transported by fibers of passage. Brain Res 674:107–111PubMedCrossRefGoogle Scholar
  31. Chen YW, Rada PV, Bützler BP, Leibowitz SF, Hoebel BG (2012) Corticotropin-releasing factor in the nucleus accumbens shell induces swim depression, anxiety, and anhedonia along with changes in local dopamine/acetylcholine balance. Neuroscience 206:155–166PubMedCrossRefGoogle Scholar
  32. Cholvin T, Loureiro M, Cassel R, Cosquer B, Geiger K, De Sa Nogueira D, Raingard H, Robelin L, Kelche C, Pereira de Vasconcelos A, Cassel JC (2013) The ventral midline thalamus contributes to strategy shifting in a memory task requiring both prefrontal cortical and hippocampal functions. J Neurosci 33:8772–8783PubMedCrossRefGoogle Scholar
  33. Churchwell JC, Morris AM, Heurtelou NM, Kesner RP (2009) Interactions between the prefrontal cortex and amygdala during delay discounting and reversal. Behav Neurosci 123:1185–1196PubMedPubMedCentralCrossRefGoogle Scholar
  34. Ciocchi S, Herry C, Grenier F, Wolff SBE, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Muller C, Luthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277–282PubMedCrossRefGoogle Scholar
  35. Clarke HF, Robbins TW, Roberts AC (2008) Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 28:10972–10982PubMedPubMedCentralCrossRefGoogle Scholar
  36. Crestani CC, Alves FH, Gomes FV, Resstel LB, Correa FM, Herman JP (2013) Mechanisms in the bed nucleus of the stria terminalis involved in control of autonomic and neuroendocrine functions: a review. Curr Neuropharmacol 11:141–159PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dado RJ, Burstein R, Cliffer KD, Giesler GJ Jr (1990) Evidence that Fluoro-Gold can be transported avidly through fibers of passage. Brain Res 533:329–333PubMedCrossRefGoogle Scholar
  38. Davis M, Shi C (1999) The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann N Y Acad Sci 877:281–291PubMedCrossRefGoogle Scholar
  39. Davis M, Walker DL (2013) Role of bed nucleus of the stria terminalis and amygdala AMPA receptors in the development and expression of context conditioning and sensitization of startle by prior shock. Brain Struct Funct 219:1969–1982PubMedPubMedCentralCrossRefGoogle Scholar
  40. Davis M, Walker DL, Miles L, Grillon C (2010) Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacol 35:105–135CrossRefGoogle Scholar
  41. de Bruin JP, Sanchez-Santed F, Heinsbroek RP, Donker A, Postmes P (1994) A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 652:323–333PubMedCrossRefGoogle Scholar
  42. deCampo DM, Fudge JL (2013) Amygdala projections to the lateral bed nucleus of the stria terminalis in the macaque: comparison with ventral striatal afferents. J Comp Neurol 521:3191–3216PubMedCrossRefGoogle Scholar
  43. Dias R, Aggleton JP (2000) Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 12:4457–4466PubMedCrossRefGoogle Scholar
  44. Difeliceantonio AG, Berridge KC (2012) Which cue to ‘want’? Opioid stimulation of central amygdala makes goal-trackers show stronger goal-tracking, just as sign-trackers show stronger sign-tracking. Behav Brain Res 230:399–408PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475–477PubMedCrossRefGoogle Scholar
  46. Donovan MK, Wyss JM (1983) Evidence for some collateralization between cortical and diencephalic efferent axons of the rat subicular cortex. Brain Res 259:181–192PubMedCrossRefGoogle Scholar
  47. Duvarci S, Bauer EP, Paré D (2009) The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 29:10357–10361PubMedPubMedCentralCrossRefGoogle Scholar
  48. Elharrar E, Warhaftig G, Issler O, Sztainberg Y, Dikshtein Y, Zahut R, Redlus L, Chen A, Yadid G (2013) Overexpression of corticotropin-releasing factor receptor type 2 in the bed nucleus of stria terminalis improves posttraumatic stress disorder-like symptoms in a model of incubation of fear. Biol Psychiatry 74:827–836PubMedCrossRefGoogle Scholar
  49. Fendt M, Fanselow MS (1999) The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23:743–760PubMedCrossRefGoogle Scholar
  50. Ferrier D (1876/1966) The functions of the brain. Smith Elder, London, 1876 (reprinted in 1966 by Dawsons of Pall Mall, London) Google Scholar
  51. Floresco SB, Magyar O, Ghods-Sharifi S, Vexelman C, Tse MT (2006) Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacol 31:297–309CrossRefGoogle Scholar
  52. Floresco SB, Zhang Y, Enomoto T (2009) Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 204:396–409PubMedCrossRefGoogle Scholar
  53. Gallagher M, Holland PC (1994) The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA 91:11771–11776PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gallagher M, Graham PW, Holland PC (1990) The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior. J Neurosci 10:1906–1911PubMedGoogle Scholar
  55. Garris PA, Christensen JR, Rebec GV, Wightman RM (1997) Real-time measurement of electrically evoked extracellular dopamine in the striatum of freely moving rats. J Neurochem 68:152–161PubMedCrossRefGoogle Scholar
  56. Groenewegen HJ, Vermeulen-Van der Zee E, te Kortschot A, Witter MP (1987) Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience 23:103–120PubMedCrossRefGoogle Scholar
  57. Groenewegen HJ, Berendse HW, Wolters JG, Lohman AH (1990) The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog Brain Res 85:95–118PubMedCrossRefGoogle Scholar
  58. Groenewegen HJ, Wright CI, Uylings HB (1997) The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J Psychopharmacol 11:99–106PubMedCrossRefGoogle Scholar
  59. Guarraci FA, Frohardt RJ, Young SL, Kapp BS (1999a) A functional role for dopamine transmission in the amygdala during conditioned fear. Ann N Y Acad Sci 877:732–736PubMedCrossRefGoogle Scholar
  60. Guarraci FA, Frohardt RJ, Kapp BS (1999b) Amygdaloid D-1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827:28–40PubMedCrossRefGoogle Scholar
  61. Guarraci FA, Frohardt RJ, Falls WA, Kapp BS (2000) The effects of intra-amygdaloid infusions of a D2 dopamine receptor antagonist on Pavlovian fear conditioning. Behav Neurosci 114:647–651PubMedCrossRefGoogle Scholar
  62. Gungor NZ, Paré D (2016) Functional heterogeneity in the bed nucleus of the stria terminalis. J Neurosci 36:8038–8049PubMedPubMedCentralCrossRefGoogle Scholar
  63. Hamilton DA, Brigman JL (2015) Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav 14:4–21PubMedPubMedCentralCrossRefGoogle Scholar
  64. Haralambous T, Westbrook RF (1999) An infusion of bupivacaine into the nucleus accumbens disrupts the acquisition, but not the expression, of contextual fear conditioning. Behav Neurosci 113:925–940PubMedCrossRefGoogle Scholar
  65. Harris GW (1958) Chairman’s opening remarks. In: Wolstenholme GEW, O’Connor CM (eds) Ciba foundation symposium on the neurological basis of behavior. J & A Churchill, LTD, London, pp 1–3Google Scholar
  66. Haubensak W, Kunwar PS, Cai HJ, Ciocchi S, Wall NR, Ponnusamy R, Biag J, Dong HW, Deisseroth K, Callaway EM, Fanselow MS, Luthi A, Anderson DJ (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468:270–276PubMedPubMedCentralCrossRefGoogle Scholar
  67. Haufler D, Nagy FZ, Paré D (2013) Neuronal correlates of fear conditioning in the bed nucleus of the stria terminalis. Learn Mem (Cold Spring Harbor, NY) 20(11):633–641CrossRefGoogle Scholar
  68. Heimer L (1972) The olfactory connections of the diencephalon in the rat. An experimental light- and electron-microscopic study with special emphasis on the problem of terminal degeneration. Brain Behav Evol 6:484–523PubMedCrossRefGoogle Scholar
  69. Heimer L (2003) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160:1726–1739PubMedCrossRefGoogle Scholar
  70. Heimer L, Alheid GF (1991) Piecing together the puzzle of basal forebrain anatomy. In: Napier TC, Kalivas PW, Hanin I (eds) The basal forebrain: anatomy to function. Plenum Press, New York, pp 1–42CrossRefGoogle Scholar
  71. Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147PubMedCrossRefGoogle Scholar
  72. Heimer L, Wilson RD (1975) The subcortical projections of allocortex: similarities in the neuronal associations of the hippocampus, the piriform cortex and the neocortex. In: Santini M (ed) Golgi centennial symposium proceedings. Raven Press, New York, pp 173–193Google Scholar
  73. Heimer L, de Olmos J, Alheid GF, Zaborszky L (1991) “Perestroika” in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 87:109–165PubMedCrossRefGoogle Scholar
  74. Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, Zahm DS (1997a) The accumbens: beyond the core-shell dichotomy. J Neuropsychiatr Clin Neurosci 9:354–381CrossRefGoogle Scholar
  75. Heimer L, Harlan RE, Alheid GF, Garcia MM, de Olmos JS (1997b) Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience 76:957–1006PubMedCrossRefGoogle Scholar
  76. Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854–857PubMedCrossRefGoogle Scholar
  77. Holstege G (1991) Descending motor pathways and the spinal motor system: limbic and non-limbic components. Prog Brain Res 87:307–421PubMedCrossRefGoogle Scholar
  78. Holstege G (1992) The emotional motor system. Eur J Morphol 30:67–79PubMedGoogle Scholar
  79. Holstege G, Bandler R, Saper CB (eds) (1996) The emotional motor system. Progress in brain research, vol 107. Elsevier, Amsterdam, pp 3–6CrossRefGoogle Scholar
  80. Holstege GG, Mouton LJ, Gerrits MN (2004) Emotional motor system. In: Paxinos G, Mai JK (eds) The human nervous system. Elsevier, Amsterdam, pp 1306–1324CrossRefGoogle Scholar
  81. Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651–656PubMedCrossRefGoogle Scholar
  82. Ide S, Hara T, Ohno A, Tamano R, Koseki K, Naka T, Maruyama C, Kaneda K, Yoshioka M, Minami M (2013) Opposing roles of corticotropin-releasing factor and neuropeptide Y within the dorsolateral bed nucleus of the stria terminalis in the negative affective component of pain in rats. J Neurosci 33:5881–5894PubMedCrossRefGoogle Scholar
  83. Jakab RL, Leranth C (1995) Septum. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 405–442Google Scholar
  84. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS (2009) 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. J Comp Neurol 513:566–596PubMedPubMedCentralCrossRefGoogle Scholar
  85. Jolkkonen E, Miettinen R, Pitkanen A (2001) Projections from the amygdalo-piriform transition area to the amygdaloid complex: a PHA-l study in rat. J Comp Neurol 432:440–465PubMedCrossRefGoogle Scholar
  86. Jones BF, Groenewegen HJ, Witter MP (2005) Intrinsic connections of the cingulate cortex in the rat suggest the existence of multiple functionally segregated networks. Neuroscience 133:193–207PubMedCrossRefGoogle Scholar
  87. Kalivas PW, Barnes CD (eds) (1993) Limbic motor circuits and neuropsychiatry. CRC Press, Boca RatonGoogle Scholar
  88. Kelley AE, Smith-Roe SL, Holahan MR (1997) Response-reinforcement learning is dependent on N-methyl-d-aspartate receptor activation in the nucleus accumbens core. Proc Natl Acad Sci USA 94:12174–12179PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kelly PH, Seviour PW, Iversen SD (1975) Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res 94:507–522PubMedCrossRefGoogle Scholar
  90. Killcross S, Robbins TW, Everitt BJ (1997) Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388:377–380PubMedCrossRefGoogle Scholar
  91. Kim HD, Hesterman J, Call T, Magazu S, Keeley E, Armenta K, Kronman H, Neve RL, Nestler EJ, Ferguson D (2016) SIRT1 mediates depression-like behaviors in the nucleus accumbens. J Neurosci 36:8441–8452PubMedPubMedCentralCrossRefGoogle Scholar
  92. Knapska E, Lioudyno V, Kiryk A, Mikosz M, Gorkiewicz T, Michaluk P, Gawlak M, Chaturvedi M, Mochol G, Balcerzyk M, Wojcik DK, Wilczynski GM, Kaczmarek L (2013) Reward learning requires activity of matrix metalloproteinase-9 in the central amygdala. J Neurosci 33:14591–14600PubMedCrossRefGoogle Scholar
  93. Koob GF, Sanna PP, Bloom FE (1998) Neuroscience of addiction. Neuron 21:467–476PubMedCrossRefGoogle Scholar
  94. Kosaki Y, Watanabe S (2012) Dissociable roles of the medial prefrontal cortex, the anterior cingulate cortex, and the hippocampus in behavioural flexibility revealed by serial reversal of three-choice discrimination in rats. Behav Brain Res 227:81–90PubMedCrossRefGoogle Scholar
  95. Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225–254PubMedCrossRefGoogle Scholar
  96. Lanser MG, Ellenbroek BA, Zitman FG, Heeren DJ, Cools AR (2001) The role of medial prefrontal cortical dopamine in spontaneous flexibility in the rat. Behav Pharmacol 12:163–171PubMedCrossRefGoogle Scholar
  97. LeDoux JE (1995) Emotion: clues from the brain. Ann Rev Psychol 46:209–235CrossRefGoogle Scholar
  98. LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184PubMedCrossRefGoogle Scholar
  99. Lee HJ, Groshek F, Petrovich GD, Cantalini JP, Gallagher M, Holland PC (2005) Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J Neurosci 25:3881–3888PubMedPubMedCentralCrossRefGoogle Scholar
  100. Lee HJ, Youn JM, O MJ, Gallagher M, Holland PC (2006) Role of substantia nigra–amygdala connections in surprise-induced enhancement of attention. J Neurosci 26:6077–6081PubMedCrossRefGoogle Scholar
  101. Lee HJ, Youn JM, Gallagher M, Holland PC (2008) Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning. Eur J Neurosci 27(11):3043–3049PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lee HJ, Gallagher M, Holland PC (2010) The central amygdala projection to the substantia nigra reflects prediction error information in appetitive conditioning. Learn Mem (Cold Spring Harbor, NY) 17:531–538CrossRefGoogle Scholar
  103. Leknes S, Tracey I (2008) Science and society—A common neurobiology for pain and pleasure. Nat Rev Neurosci 9:314–320PubMedCrossRefGoogle Scholar
  104. Levita L, Dalley JW, Robbins TW (2002) Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core. Behav Neurosci 116:539–552PubMedCrossRefGoogle Scholar
  105. Li HH, Penzo MA, Taniguchi H, Kopec CD, Huang ZJ, Li B (2013) Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci 16:332–339PubMedPubMedCentralCrossRefGoogle Scholar
  106. MacLean PD (1989) The triune brain in evolution: role in paleocerebral functions. Plenum Press, New YorkGoogle Scholar
  107. Mahler SV, Berridge KC (2012) What and when to “want”? Amygdala-based focusing of incentive salience upon sugar and sex. Psychopharmacol 221:407–426CrossRefGoogle Scholar
  108. Mala H, Andersen LG, Christensen RF, Felbinger A, Hagstrom J, Meder D, Pearce H, Mogensen J (2015) Prefrontal cortex and hippocampus in behavioural flexibility and posttraumatic functional recovery: reversal learning and set-shifting in rats. Brain Res Bull 116:34–44PubMedCrossRefGoogle Scholar
  109. Maren S (2005a) Building and burying fear memories in the brain. Neuroscientist 11:89–99PubMedCrossRefGoogle Scholar
  110. Maren S (2005b) Synaptic mechanisms of associative memory in the amygdala. Neuron 47(6):783–786PubMedCrossRefGoogle Scholar
  111. Martin LJ, Powers RE, Dellovade TL, Price DL (1991) The bed nucleus-amygdala continuum in human and monkey. J Comp Neurol 309:445–485PubMedCrossRefGoogle Scholar
  112. McCutcheon JE, Ebner SR, Loriaux AL, Roitman MF (2012) Encoding of aversion by dopamine and the nucleus accumbens. Front Neurosci 6:137PubMedPubMedCentralCrossRefGoogle Scholar
  113. McDannald MA (2010) Contributions of the amygdala central nucleus and ventrolateral periaqueductal grey to freezing and instrumental suppression in Pavlovian fear conditioning. Behav Brain Res 211:111–117PubMedPubMedCentralCrossRefGoogle Scholar
  114. McDonald AJ (1991a) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1–14PubMedCrossRefGoogle Scholar
  115. McDonald AJ (1991b) Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44:15–33PubMedCrossRefGoogle Scholar
  116. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332PubMedCrossRefGoogle Scholar
  117. McDonald AJ (2003) Is there an amygdala and how far does it extend? Ann N Y Acad Sci 985:1–21PubMedCrossRefGoogle Scholar
  118. McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55–75PubMedCrossRefGoogle Scholar
  119. McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M (1999) Cortical afferents to the extended amygdala. Ann N Y Acad Sci 877:309–338PubMedCrossRefGoogle Scholar
  120. McGeorge AJ, Faull RLM (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503–537PubMedCrossRefGoogle Scholar
  121. McGinty JF (ed) (1999) Advancing from the ventral striatum to the extended amygdala. Ann NY Acad Sci 877, New YorkGoogle Scholar
  122. McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol 369:302–318PubMedCrossRefGoogle Scholar
  123. Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language and memory. Ann Neurol 28:597–613PubMedCrossRefGoogle Scholar
  124. Miller SS, Urcelay GP (2007) The central amygdala joins the lateral amygdala in the fear memory party. J Neurosci 27:2151–2152PubMedCrossRefGoogle Scholar
  125. Naber PA, Witter MP (1998) Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284–297PubMedCrossRefGoogle Scholar
  126. Nader K, Ledoux JE (1997) Is it time to invoke multiple fear learning systems in the amygdala? Trends Cogn Sci 1:241–244PubMedCrossRefGoogle Scholar
  127. Nagai MM, Gomes FV, Crestani CC, Resstel LB, Joca SR (2013) Noradrenergic neurotransmission within the bed nucleus of the stria terminalis modulates the retention of immobility in the rat forced swimming test. Behav Pharmacol 24:214–221PubMedCrossRefGoogle Scholar
  128. Napier TC, Kalivas PW, Hanin I (eds) (1991) The basal forebrain: anatomy to function, vol. 295. Adv Exp Med Biol, Plenum Press, New YorkGoogle Scholar
  129. Nestler EJ, Carlezon WA Jr (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159PubMedCrossRefGoogle Scholar
  130. Neugebauer V, Li W, Bird GC, Han JS (2004) The amygdala and persistent pain. Neuroscientist 10:221–234PubMedCrossRefGoogle Scholar
  131. Oler JA, Tromp DP, Fox AS, Kovner R, Davidson RJ, Alexander AL, McFarlin DR, Birn RM, Berg EB, deCampo DM, Kalin NH, Fudge JL (2016) Connectivity between the central nucleus of the amygdala and the bed nucleus of the stria terminalis in the non-human primate: neuronal tract tracing and developmental neuroimaging studies. Brain Struct Funct. doi: 10.1007/s00429-016-1198-9
  132. Öngür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10(206):219Google Scholar
  133. Paré D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1–9PubMedCrossRefGoogle Scholar
  134. Parkinson JA, Robbins TW, Everitt BJ (1999) Selective excitotoxic lesions of the nucleus accumbens core and shell differentially affect aversive Pavlovian conditioning to discrete and contextual cues. Psychobiol 27:256–266Google Scholar
  135. Pascoe JP, Kapp BS (1985) Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 16:117–133PubMedCrossRefGoogle Scholar
  136. Pettit HO, Ettenberg A, Bloom FE, Koob GF (1984) Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacol 84:167–173CrossRefGoogle Scholar
  137. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187PubMedCrossRefGoogle Scholar
  138. Poulos AM, Li V, Sterlace SS, Tokushige F, Ponnusamy R, Fanselow MS (2009) Persistence of fear memory across time requires the basolateral amygdala complex. PNAS, USA 106:11737–11741CrossRefGoogle Scholar
  139. Ragozzino ME (2002) The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learn Mem (Cold Spring Harbor, NY) 9:18–28CrossRefGoogle Scholar
  140. Ragozzino ME (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121:355–375PubMedCrossRefGoogle Scholar
  141. Ragozzino ME, Rozman S (2007) The effect of rat anterior cingulate inactivation on cognitive flexibility. Behav Neurosci 121:698–706PubMedCrossRefGoogle Scholar
  142. Ragozzino ME, Detrick S, Kesner RP (1999) Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19:4585–4594PubMedGoogle Scholar
  143. Rebec GV, Christensen JR, Guerra C, Bardo MT (1997) Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty. Brain Res 776:61–67PubMedCrossRefGoogle Scholar
  144. Reynolds SM, Berridge KC (2001) Fear and feeding in the nucleus accumbens shell: rostrocaudal segregation of GABA-elicited defensive behavior versus eating behavior. J Neurosci 21:3261–3270PubMedGoogle Scholar
  145. Reynolds SM, Berridge KC (2008) Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 11:423–425PubMedPubMedCentralCrossRefGoogle Scholar
  146. Reynolds SM, Zahm DS (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25:11757–11767PubMedCrossRefGoogle Scholar
  147. Richard JM, Berridge KC (2011a) Metabotropic glutamate receptor blockade in nucleus accumbens shell shifts affective valence towards fear and disgust. Eur J Neurosci 33:736–747PubMedCrossRefGoogle Scholar
  148. Richard JM, Berridge KC (2011b) Nucleus accumbens dopamine/glutamate interaction switches modes to generate desire versus dread: d1 alone for appetitive eating but D1 and D2 together for fear. J Neurosci 31:12866–12879PubMedPubMedCentralCrossRefGoogle Scholar
  149. Richard JM, Castro DC, Difeliceantonio AG, Robinson MJ, Berridge KC (2013) Mapping brain circuits of reward and motivation: in the footsteps of Ann Kelley. Neurosci Biobehav Rev 37:1919–1931PubMedCrossRefGoogle Scholar
  150. Riedel G, Harrington NR, Hall G, Macphail EM (1997) Nucleus accumbens lesions impair context, but not cue, conditioning in rats. NeuroReport 8:2477–2481PubMedCrossRefGoogle Scholar
  151. Risold PY, Swanson LW (1997a) Chemoarchitecture of the rat lateral septal nucleus. Brain Res Rev 24:91–113PubMedCrossRefGoogle Scholar
  152. Risold PY, Swanson LW (1997b) Connections of the rat lateral septal complex. Brain Res Rev 24:115–195PubMedCrossRefGoogle Scholar
  153. Roberts DCS, Koob GF, Klonoff P, Fibiger HC (1980) Extinction and recovery of cocaine self-administration following 6-hydroxydopamine lesions of the nucleus accumbens. Pharmacol Biochem Behav 12:781–787PubMedCrossRefGoogle Scholar
  154. Robinson S, Sandstrom SM, Denenberg VH, Palmiter RD (2005) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav Neurosci 119:5–15PubMedCrossRefGoogle Scholar
  155. Rogan MT, LeDoux JE (1996) Emotion: systems, cells, synaptic plasticity. Cell 85(4):469–475PubMedCrossRefGoogle Scholar
  156. Rouwette T, Vanelderen P, Roubos EW, Kozicz T, Vissers K (2012) The amygdala, a relay station for switching on and off pain. Eur J Pain ((London, England)) 16:782–792CrossRefGoogle Scholar
  157. Santiago AC, Shammah-Lagnado SJ (2005) Afferent connections of the amygdalopiriform transition area in the rat. J Comp Neurol 489:349–371PubMedCrossRefGoogle Scholar
  158. Saper CB (1996) Role of the cerebral cortex and striatum in emotional motor response. Prog Brain Res 107:537–550PubMedCrossRefGoogle Scholar
  159. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599PubMedCrossRefGoogle Scholar
  160. Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063–1073PubMedCrossRefGoogle Scholar
  161. Shackman AJ, Fox AS (2016) Contributions of the central extended amygdala to fear and anxiety. J Neurosci 36:8050–8063PubMedPubMedCentralCrossRefGoogle Scholar
  162. Shammah-Lagnado SJ, Santiago AC (1999) Projections of the amygdalopiriform transition area (APir). A PHA-L study in the rat. Ann N York Acad Sci 877:655–660CrossRefGoogle Scholar
  163. Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Rev 46:71–117PubMedCrossRefGoogle Scholar
  164. Shi CJ, Cassell MD (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399:440–468PubMedCrossRefGoogle Scholar
  165. Silberman Y, Winder DG (2013) Emerging role for corticotropin releasing factor signaling in the bed nucleus of the stria terminalis at the intersection of stress and reward. Front Psychiatry 4:42PubMedPubMedCentralCrossRefGoogle Scholar
  166. Skorzewska A, Bidzinski A, Hamed A, Lehner M, Turzynska D, Sobolewska A, Szyndler J, Maciejak P, Wislowska-Stanek A, Plaznik A (2009) The effect of CRF and alpha-helical CRF(9-41) on rat fear responses and amino acids release in the central nucleus of the amygdala. Neuropharmacol 57:148–156CrossRefGoogle Scholar
  167. Smith-Roe SL, Kelley AE (2000) Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20:7737–7742PubMedGoogle Scholar
  168. Stalnaker TA, Franz TM, Singh T, Schoenbaum G (2007) Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 54:51–58PubMedCrossRefGoogle Scholar
  169. Sun N, Yi H, Cassell MD (1994) Evidence for a GABAergic interface between cortical afferents and brainstem projection neurons in the rat central extended amygdala. J Comp Neurol 340:43–64PubMedCrossRefGoogle Scholar
  170. Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113–164PubMedCrossRefGoogle Scholar
  171. Swanson LW (2003) The amygdala and its place in the cerebral hemisphere. Ann N Y Acad Sci 985:174–184PubMedCrossRefGoogle Scholar
  172. Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331PubMedCrossRefGoogle Scholar
  173. Swanson LW, Sawchenko PE, Cowan WM (1981) Evidence for collateral projections by neurons in Ammon’s horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat. J Neurosci 1:548–559PubMedGoogle Scholar
  174. Tait DS, Brown VJ (2007) Difficulty overcoming learned non-reward during reversal learning in rats with ibotenic acid lesions of orbital prefrontal cortex. Ann N Y Acad Sci 1121:407–420PubMedCrossRefGoogle Scholar
  175. Taylor JR, Robbins TW (1984) Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacol 84:405–412CrossRefGoogle Scholar
  176. Taylor JR, Robbins TW (1986) 6-hydroxydopamine lesions of the nucleus accumbens, but not of the caudate nucleus, attenuate enhanced responding with reward-related stimuli produced by intra-accumbens d-amphetamine. Psychopharmacol 90:390–397CrossRefGoogle Scholar
  177. Walker DL, Davis M (2008) Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer. Brain Struct Funct 213:29–42PubMedCrossRefGoogle Scholar
  178. Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463:199–216PubMedCrossRefGoogle Scholar
  179. Walker DL, Miles LA, Davis M (2009) Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 33:1291–1308PubMedPubMedCentralCrossRefGoogle Scholar
  180. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, Iniguez SD, Cao JL, Kirk A, Chakravarty S, Kumar A, Krishnan V, Neve RL, Cooper DC, Bolanos CA, Barrot M, McClung CA, Nestler EJ (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12:200–209PubMedPubMedCentralCrossRefGoogle Scholar
  181. Wickens J, Kotter R (1995) Cellular models of reinforcement. In: Houk JC, Davis JL, Beiser DG (eds) Models of information processing in the basal Ganglia. MIT Press, Cambridge, pp 187–214Google Scholar
  182. Wilensky AE, Schafe GE, Kristensen MP, LeDoux JE (2006) Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 26:12387–12396PubMedCrossRefGoogle Scholar
  183. Will MJ, Franzblau EB, Kelley AE (2004) The amygdala is critical for opioid-mediated binge eating of fat. NeuroReport 15:1857–1860PubMedCrossRefGoogle Scholar
  184. Wise RA (1985) The anhedonia hypothesis: Mark III. Behav Brain Sci 8:178–186CrossRefGoogle Scholar
  185. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494PubMedCrossRefGoogle Scholar
  186. Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14:169–183PubMedPubMedCentralCrossRefGoogle Scholar
  187. Woods JW (1964) Behavior of chronic decerebrate rats. J Neurophysiol 27:635–644PubMedGoogle Scholar
  188. Yeterian EH, Van Hoesen GW (1978) Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res 139:43–63PubMedCrossRefGoogle Scholar
  189. Yetnikoff L, Lavezzi HN, Reichard RA, Zahm DS (2014a) An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 282C:23–48CrossRefGoogle Scholar
  190. Yetnikoff L, Reichard RA, Schwartz ZM, Parsely KP, Zahm DS (2014b) Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat. J Comp Neurol 522:1031–1047PubMedPubMedCentralCrossRefGoogle Scholar
  191. Yetnikoff L, Cheng AY, Lavezzi HN, Parsley KP, Zahm DS (2015) Sources of input to the rostromedial tegmental nucleus, ventral tegmental area, and lateral habenula compared: a study in rat. J Comp Neurol 523:2426–2456PubMedPubMedCentralCrossRefGoogle Scholar
  192. Yokel RA, Wise RA (1975) Increased lever pressing for amphetamine after pimozide in rats: implications for a dopamine theory of reward. Science 187:547–549PubMedCrossRefGoogle Scholar
  193. Yokel RA, Wise RA (1976) Attenuation of intravenous amphetamine reinforcement by central dopamine blockade in rats. Psychopharmacol 48:311–318CrossRefGoogle Scholar
  194. Zahm DS (1998) Is the caudomedial shell of the nucleus accumbens part of the extended amygdala? A consideration of connections. Crit Rev Neurobiol 12:245–265PubMedCrossRefGoogle Scholar
  195. Zahm DS (2000) An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev 24:85–105PubMedCrossRefGoogle Scholar
  196. Zahm DS (2006) The evolving theory of basal forebrain functional-anatomical “macrosystems.”. Neurosci Biobehav Rev 30(2):148–172PubMedCrossRefGoogle Scholar
  197. Zahm DS (2008a) Chapter 5: cooperation and competition of macrosystem outputs. In: Heimer L, Van Hoesen GW, Trimble M, Zahm DS (eds) Anatomy of neuropsychiatry: the new anatomy of the basal forebrain and its implications for neuropsychiatric disease. Elsevier, Amsterdam, pp 101–139Google Scholar
  198. Zahm DS (2008b) Accumbens in a functional-anatomical systems context. In: David H (ed) The nucleus accumbens: neurotransmitters and related behaviours. Transworld Research Network-Research Signpost, Kerala, pp 1–37Google Scholar
  199. Zahm DS, Grosu S, Irving JC, Williams EA (2003) Discrimination of striatopallidum and extended amygdala in the rat: a role for parvalbumin immunoreactive neurons? Brain Res 978:141–154PubMedCrossRefGoogle Scholar
  200. Zahm DS, Schwartz ZM, Lavezzi HN, Yetnikoff L, Parsley KP (2014) Comparison of the locomotor-activating effects of bicuculline infusions into the preoptic area and ventral pallidum. Brain Struct Funct 219:511–526PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Pharmacological and Physiological Science, School of MedicineSaint Louis UniversitySaint LouisUSA

Personalised recommendations