Skip to main content
Log in

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

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. Consistent with ample considerations described elsewhere (Alheid and Heimer 1988; Carlssen and Heimer 1988), basal amygdala will be treated in this paper as a cortical-like structure.

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

References

  • Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985:185–205

    Article  CAS  PubMed  Google Scholar 

  • 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 27:1–39

    Article  CAS  PubMed  Google Scholar 

  • 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 285:208–215

    CAS  PubMed  Google Scholar 

  • Altier N, Stewart J (1999) The role of dopamine in the nucleus accumbens in analgesia. Life Sci 65:2269–2287

    Article  CAS  PubMed  Google Scholar 

  • Amorapanth P, LeDoux JE, Nader K (2000) Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 3:74–79

    Article  CAS  PubMed  Google Scholar 

  • 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) 21:223–231

    Article  Google Scholar 

  • Bard P (1928) A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am J Physiol 84:490–515

    Google Scholar 

  • 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 55–75

    Google Scholar 

  • 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 99:11435–11440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102:8357–8362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 316:314–347

    Article  CAS  PubMed  Google Scholar 

  • Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacol 191:391–431

    Article  CAS  Google Scholar 

  • Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28:309–369

    Article  CAS  PubMed  Google Scholar 

  • Berridge KC, Robinson TE, Aldridge JW (2009) Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr Opin Pharmacol 9:65–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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) 17:1625–1636

    Google Scholar 

  • 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 179:219–228

    Article  PubMed  Google Scholar 

  • 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 338:255–278

    Article  CAS  PubMed  Google Scholar 

  • 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 40:245–251

    Article  CAS  PubMed  Google Scholar 

  • 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 15:2301–2311

    CAS  PubMed  Google Scholar 

  • Cannon WB, Britton SW (1927) Pseudoaffective medulloadrenal secretion. Am J Physiol 79:4333–4465

    Google Scholar 

  • Cannon CM, Palmiter RD (2003) Reward without dopamine. J Neurosci 23:10827–10831

    CAS  PubMed  Google Scholar 

  • 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 324:180–194

    Article  CAS  PubMed  Google Scholar 

  • 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) 282:2272–2275

    Article  CAS  Google Scholar 

  • Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436–445

    Article  CAS  PubMed  Google Scholar 

  • Carlssen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380

    Article  Google Scholar 

  • Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641

    Article  CAS  PubMed  Google Scholar 

  • Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179–207

    Article  CAS  PubMed  Google Scholar 

  • Cassell MD (1998) The amygdala: myth or monolith? Trends Neurosci 21:200–201

    Article  CAS  PubMed  Google Scholar 

  • Cassell MD, Freedman LJ, Shi C (1999) The intrinsic organization of the central extended amygdala. Ann N Y Acad Sci 877:217–241

    Article  CAS  PubMed  Google Scholar 

  • 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 674:107–111

    Article  CAS  PubMed  Google Scholar 

  • 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 206:155–166

    Article  CAS  PubMed  Google Scholar 

  • 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 33:8772–8783

    Article  CAS  PubMed  Google Scholar 

  • Churchwell JC, Morris AM, Heurtelou NM, Kesner RP (2009) Interactions between the prefrontal cortex and amygdala during delay discounting and reversal. Behav Neurosci 123:1185–1196

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 468:277–282

    Article  CAS  PubMed  Google Scholar 

  • 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 28:10972–10982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:141–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dado RJ, Burstein R, Cliffer KD, Giesler GJ Jr (1990) Evidence that Fluoro-Gold can be transported avidly through fibers of passage. Brain Res 533:329–333

    Article  CAS  PubMed  Google Scholar 

  • 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 877:281–291

    Article  CAS  PubMed  Google Scholar 

  • 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 219:1969–1982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 35:105–135

    Article  Google Scholar 

  • 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 652:323–333

    Article  PubMed  Google Scholar 

  • 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 521:3191–3216

    Article  PubMed  Google Scholar 

  • 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 12:4457–4466

    Article  CAS  PubMed  Google Scholar 

  • 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 230:399–408

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475–477

    Article  CAS  PubMed  Google Scholar 

  • Donovan MK, Wyss JM (1983) Evidence for some collateralization between cortical and diencephalic efferent axons of the rat subicular cortex. Brain Res 259:181–192

    Article  CAS  PubMed  Google Scholar 

  • Duvarci S, Bauer EP, Paré D (2009) The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 29:10357–10361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 74:827–836

    Article  CAS  PubMed  Google Scholar 

  • Fendt M, Fanselow MS (1999) The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23:743–760

    Article  CAS  PubMed  Google Scholar 

  • Ferrier D (1876/1966) The functions of the brain. Smith Elder, London, 1876 (reprinted in 1966 by Dawsons of Pall Mall, London)

  • 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 31:297–309

    Article  CAS  Google Scholar 

  • Floresco SB, Zhang Y, Enomoto T (2009) Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 204:396–409

    Article  PubMed  Google Scholar 

  • Gallagher M, Holland PC (1994) The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA 91:11771–11776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallagher M, Graham PW, Holland PC (1990) The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior. J Neurosci 10:1906–1911

    CAS  PubMed  Google Scholar 

  • 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 68:152–161

    Article  CAS  PubMed  Google Scholar 

  • 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 23:103–120

    Article  CAS  PubMed  Google Scholar 

  • 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 85:95–118

    Article  CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Wright CI, Uylings HB (1997) The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J Psychopharmacol 11:99–106

    Article  CAS  PubMed  Google Scholar 

  • 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 877:732–736

    Article  CAS  PubMed  Google Scholar 

  • Guarraci FA, Frohardt RJ, Kapp BS (1999b) Amygdaloid D-1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827:28–40

    Article  CAS  PubMed  Google Scholar 

  • 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 114:647–651

    Article  CAS  PubMed  Google Scholar 

  • Gungor NZ, Paré D (2016) Functional heterogeneity in the bed nucleus of the stria terminalis. J Neurosci 36:8038–8049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton DA, Brigman JL (2015) Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav 14:4–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 113:925–940

    Article  CAS  PubMed  Google Scholar 

  • 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 1–3

    Google Scholar 

  • 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 468:270–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):633–641

    Article  Google Scholar 

  • 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 6:484–523

    Article  CAS  PubMed  Google Scholar 

  • Heimer L (2003) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160:1726–1739

    Article  PubMed  Google Scholar 

  • 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 1–42

    Chapter  Google Scholar 

  • Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147

    Article  PubMed  Google Scholar 

  • 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 173–193

    Google Scholar 

  • 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 87:109–165

    Article  CAS  PubMed  Google Scholar 

  • 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 9:354–381

    Article  CAS  Google Scholar 

  • 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 76:957–1006

    Article  CAS  PubMed  Google Scholar 

  • Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854–857

    Article  CAS  PubMed  Google Scholar 

  • Holstege G (1991) Descending motor pathways and the spinal motor system: limbic and non-limbic components. Prog Brain Res 87:307–421

    Article  CAS  PubMed  Google Scholar 

  • Holstege G (1992) The emotional motor system. Eur J Morphol 30:67–79

    CAS  PubMed  Google Scholar 

  • Holstege G, Bandler R, Saper CB (eds) (1996) The emotional motor system. Progress in brain research, vol 107. Elsevier, Amsterdam, pp 3–6

    Book  Google Scholar 

  • Holstege GG, Mouton LJ, Gerrits MN (2004) Emotional motor system. In: Paxinos G, Mai JK (eds) The human nervous system. Elsevier, Amsterdam, pp 1306–1324

    Chapter  Google Scholar 

  • Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651–656

    Article  CAS  PubMed  Google Scholar 

  • 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 33:5881–5894

    Article  CAS  PubMed  Google Scholar 

  • Jakab RL, Leranth C (1995) Septum. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 405–442

    Google Scholar 

  • 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 513:566–596

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 432:440–465

    Article  CAS  PubMed  Google Scholar 

  • 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 133:193–207

    Article  CAS  PubMed  Google Scholar 

  • Kalivas PW, Barnes CD (eds) (1993) Limbic motor circuits and neuropsychiatry. CRC Press, Boca Raton

    Google Scholar 

  • 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 94:12174–12179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 94:507–522

    Article  CAS  PubMed  Google Scholar 

  • Killcross S, Robbins TW, Everitt BJ (1997) Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388:377–380

    Article  CAS  PubMed  Google Scholar 

  • 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 36:8441–8452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:14591–14600

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, Sanna PP, Bloom FE (1998) Neuroscience of addiction. Neuron 21:467–476

    Article  CAS  PubMed  Google Scholar 

  • 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 227:81–90

    Article  PubMed  Google Scholar 

  • Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225–254

    Article  CAS  PubMed  Google Scholar 

  • 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 12:163–171

    Article  CAS  PubMed  Google Scholar 

  • LeDoux JE (1995) Emotion: clues from the brain. Ann Rev Psychol 46:209–235

    Article  CAS  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184

    Article  CAS  PubMed  Google Scholar 

  • 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 25:3881–3888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 26:6077–6081

    Article  CAS  PubMed  Google Scholar 

  • 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):3043–3049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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) 17:531–538

    Article  Google Scholar 

  • Leknes S, Tracey I (2008) Science and society—A common neurobiology for pain and pleasure. Nat Rev Neurosci 9:314–320

    Article  CAS  PubMed  Google Scholar 

  • Levita L, Dalley JW, Robbins TW (2002) Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core. Behav Neurosci 116:539–552

    Article  PubMed  Google Scholar 

  • Li HH, Penzo MA, Taniguchi H, Kopec CD, Huang ZJ, Li B (2013) Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci 16:332–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacLean PD (1989) The triune brain in evolution: role in paleocerebral functions. Plenum Press, New York

    Google Scholar 

  • Mahler SV, Berridge KC (2012) What and when to “want”? Amygdala-based focusing of incentive salience upon sugar and sex. Psychopharmacol 221:407–426

    Article  CAS  Google Scholar 

  • 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 116:34–44

    Article  PubMed  Google Scholar 

  • Maren S (2005a) Building and burying fear memories in the brain. Neuroscientist 11:89–99

    Article  PubMed  Google Scholar 

  • Maren S (2005b) Synaptic mechanisms of associative memory in the amygdala. Neuron 47(6):783–786

    Article  CAS  PubMed  Google Scholar 

  • Martin LJ, Powers RE, Dellovade TL, Price DL (1991) The bed nucleus-amygdala continuum in human and monkey. J Comp Neurol 309:445–485

    Article  CAS  PubMed  Google Scholar 

  • McCutcheon JE, Ebner SR, Loriaux AL, Roitman MF (2012) Encoding of aversion by dopamine and the nucleus accumbens. Front Neurosci 6:137

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 211:111–117

    Article  PubMed  PubMed Central  Google Scholar 

  • McDonald AJ (1991a) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1–14

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (1991b) Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44:15–33

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (2003) Is there an amygdala and how far does it extend? Ann N Y Acad Sci 985:1–21

    Article  PubMed  Google Scholar 

  • 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 71:55–75

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M (1999) Cortical afferents to the extended amygdala. Ann N Y Acad Sci 877:309–338

    Article  CAS  PubMed  Google Scholar 

  • McGeorge AJ, Faull RLM (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503–537

    Article  CAS  PubMed  Google Scholar 

  • McGinty JF (ed) (1999) Advancing from the ventral striatum to the extended amygdala. Ann NY Acad Sci 877, New York

  • McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol 369:302–318

    Article  CAS  PubMed  Google Scholar 

  • Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language and memory. Ann Neurol 28:597–613

    Article  CAS  PubMed  Google Scholar 

  • Miller SS, Urcelay GP (2007) The central amygdala joins the lateral amygdala in the fear memory party. J Neurosci 27:2151–2152

    Article  CAS  PubMed  Google Scholar 

  • 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 393:284–297

    Article  CAS  PubMed  Google Scholar 

  • Nader K, Ledoux JE (1997) Is it time to invoke multiple fear learning systems in the amygdala? Trends Cogn Sci 1:241–244

    Article  CAS  PubMed  Google Scholar 

  • 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 24:214–221

    Article  CAS  PubMed  Google Scholar 

  • Napier TC, Kalivas PW, Hanin I (eds) (1991) The basal forebrain: anatomy to function, vol. 295. Adv Exp Med Biol, Plenum Press, New York

  • Nestler EJ, Carlezon WA Jr (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159

    Article  CAS  PubMed  Google Scholar 

  • Neugebauer V, Li W, Bird GC, Han JS (2004) The amygdala and persistent pain. Neuroscientist 10:221–234

    Article  PubMed  Google Scholar 

  • 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

  • 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):219

    Google Scholar 

  • Paré D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1–9

    Article  PubMed  Google Scholar 

  • 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 27:256–266

    Google Scholar 

  • Pascoe JP, Kapp BS (1985) Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 16:117–133

    Article  CAS  PubMed  Google Scholar 

  • 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 84:167–173

    Article  CAS  Google Scholar 

  • Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187

    Article  CAS  PubMed  Google Scholar 

  • 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 106:11737–11741

    Article  CAS  Google Scholar 

  • 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) 9:18–28

    Article  Google Scholar 

  • Ragozzino ME (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121:355–375

    Article  PubMed  Google Scholar 

  • Ragozzino ME, Rozman S (2007) The effect of rat anterior cingulate inactivation on cognitive flexibility. Behav Neurosci 121:698–706

    Article  PubMed  Google Scholar 

  • 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 19:4585–4594

    CAS  PubMed  Google Scholar 

  • 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 776:61–67

    Article  CAS  PubMed  Google Scholar 

  • 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 21:3261–3270

    CAS  PubMed  Google Scholar 

  • Reynolds SM, Berridge KC (2008) Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 11:423–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds SM, Zahm DS (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25:11757–11767

    Article  CAS  PubMed  Google Scholar 

  • Richard JM, Berridge KC (2011a) Metabotropic glutamate receptor blockade in nucleus accumbens shell shifts affective valence towards fear and disgust. Eur J Neurosci 33:736–747

    Article  PubMed  Google Scholar 

  • 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 31:12866–12879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 37:1919–1931

    Article  PubMed  Google Scholar 

  • Riedel G, Harrington NR, Hall G, Macphail EM (1997) Nucleus accumbens lesions impair context, but not cue, conditioning in rats. NeuroReport 8:2477–2481

    Article  CAS  PubMed  Google Scholar 

  • Risold PY, Swanson LW (1997a) Chemoarchitecture of the rat lateral septal nucleus. Brain Res Rev 24:91–113

    Article  CAS  PubMed  Google Scholar 

  • Risold PY, Swanson LW (1997b) Connections of the rat lateral septal complex. Brain Res Rev 24:115–195

    Article  CAS  PubMed  Google Scholar 

  • 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 12:781–787

    Article  CAS  PubMed  Google Scholar 

  • Robinson S, Sandstrom SM, Denenberg VH, Palmiter RD (2005) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav Neurosci 119:5–15

    Article  CAS  PubMed  Google Scholar 

  • Rogan MT, LeDoux JE (1996) Emotion: systems, cells, synaptic plasticity. Cell 85(4):469–475

    Article  CAS  PubMed  Google Scholar 

  • 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)) 16:782–792

    Article  CAS  Google Scholar 

  • Santiago AC, Shammah-Lagnado SJ (2005) Afferent connections of the amygdalopiriform transition area in the rat. J Comp Neurol 489:349–371

    Article  PubMed  Google Scholar 

  • Saper CB (1996) Role of the cerebral cortex and striatum in emotional motor response. Prog Brain Res 107:537–550

    Article  CAS  PubMed  Google Scholar 

  • Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063–1073

    Article  CAS  PubMed  Google Scholar 

  • Shackman AJ, Fox AS (2016) Contributions of the central extended amygdala to fear and anxiety. J Neurosci 36:8050–8063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 877:655–660

    Article  CAS  Google Scholar 

  • Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Rev 46:71–117

    Article  PubMed  Google Scholar 

  • Shi CJ, Cassell MD (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399:440–468

    Article  CAS  PubMed  Google Scholar 

  • 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 4:42

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 57:148–156

    Article  CAS  Google Scholar 

  • 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 20:7737–7742

    CAS  PubMed  Google Scholar 

  • Stalnaker TA, Franz TM, Singh T, Schoenbaum G (2007) Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 54:51–58

    Article  CAS  PubMed  Google Scholar 

  • 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 340:43–64

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113–164

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW (2003) The amygdala and its place in the cerebral hemisphere. Ann N Y Acad Sci 985:174–184

    Article  PubMed  Google Scholar 

  • Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331

    Article  CAS  PubMed  Google Scholar 

  • 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 1:548–559

    CAS  PubMed  Google Scholar 

  • 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 1121:407–420

    Article  CAS  PubMed  Google Scholar 

  • Taylor JR, Robbins TW (1984) Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacol 84:405–412

    Article  CAS  Google Scholar 

  • 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 90:390–397

    Article  CAS  Google Scholar 

  • 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 213:29–42

    Article  PubMed  Google Scholar 

  • 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 463:199–216

    Article  CAS  PubMed  Google Scholar 

  • 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 33:1291–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:200–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 187–214

    Google Scholar 

  • 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 26:12387–12396

    Article  CAS  PubMed  Google Scholar 

  • Will MJ, Franzblau EB, Kelley AE (2004) The amygdala is critical for opioid-mediated binge eating of fat. NeuroReport 15:1857–1860

    Article  CAS  PubMed  Google Scholar 

  • Wise RA (1985) The anhedonia hypothesis: Mark III. Behav Brain Sci 8:178–186

    Article  Google Scholar 

  • Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494

    Article  CAS  PubMed  Google Scholar 

  • Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14:169–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Woods JW (1964) Behavior of chronic decerebrate rats. J Neurophysiol 27:635–644

    CAS  PubMed  Google Scholar 

  • Yeterian EH, Van Hoesen GW (1978) Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res 139:43–63

    Article  CAS  PubMed  Google Scholar 

  • Yetnikoff L, Lavezzi HN, Reichard RA, Zahm DS (2014a) An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 282C:23–48

    Article  CAS  Google Scholar 

  • 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 522:1031–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 523:2426–2456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokel RA, Wise RA (1975) Increased lever pressing for amphetamine after pimozide in rats: implications for a dopamine theory of reward. Science 187:547–549

    Article  CAS  PubMed  Google Scholar 

  • Yokel RA, Wise RA (1976) Attenuation of intravenous amphetamine reinforcement by central dopamine blockade in rats. Psychopharmacol 48:311–318

    Article  CAS  Google Scholar 

  • Zahm DS (1998) Is the caudomedial shell of the nucleus accumbens part of the extended amygdala? A consideration of connections. Crit Rev Neurobiol 12:245–265

    Article  CAS  PubMed  Google Scholar 

  • Zahm DS (2000) An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev 24:85–105

    Article  CAS  PubMed  Google Scholar 

  • Zahm DS (2006) The evolving theory of basal forebrain functional-anatomical “macrosystems.”. Neurosci Biobehav Rev 30(2):148–172

    Article  PubMed  Google Scholar 

  • 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 101–139

    Google Scholar 

  • 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 1–37

    Google Scholar 

  • 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 978:141–154

    Article  CAS  PubMed  Google Scholar 

  • 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 219:511–526

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Grant support: USPHS NIH NS-23805.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel S. Zahm.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reichard, R.A., Subramanian, S., Desta, M.T. et al. Abundant collateralization of temporal lobe projections to the accumbens, bed nucleus of stria terminalis, central amygdala and lateral septum. Brain Struct Funct 222, 1971–1988 (2017). https://doi.org/10.1007/s00429-016-1321-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1321-y

Keywords

Navigation