Cited by 80Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchStress Responses and Cortisol

Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats

Open access
Bienkowski, Michael S., Rinaman, Linda·2013·Brain Structure and Function

Abstract

The central nucleus of the amygdala (CEA) and lateral bed nucleus of stria terminalis (BST) are highly interconnected limbic forebrain regions that share similar connectivity with other brain regions that coordinate behavioral and physiological responses to internal and environmental stressors. Their similar connectivity is frequently referred to when describing the CEA and lateral BST together as a unified "central extended amygdala". However, the CEA and BST reportedly play distinct roles in behavioral and physiological responses associated with fear, anxiety, and social defeat, presumably due to differences in connectivity. To identify common and unique sources of input to the CEA and lateral BST, we performed dual retrograde tracing. Fluorogold and cholera toxin β were iontophoresed into the medial CEA (CEAm) and the anterior ventrolateral BST (BSTvl) of adult male rats. The anatomical distribution of tracer-labeled neurons was mapped throughout the brain. Regions with overlapping populations of CEAm- and BSTvl-projecting neurons were further examined for the presence of double-labeled neurons. Although most regions with input to the mCEA also projected to the BSTvl, and vice versa, cortical and sensory system-related regions projected more robustly to the CEAm, while motor system-related regions primarily innervated the BSTvl. The incidence of double-labeled neurons with collateralized axonal inputs to the CEAm and BSTvl was relatively small (~2 to 13%) and varied across regions, suggesting regional differences in the degree of coordinated CEAm and BSTvl input. The demonstrated similarities and differences in inputs to CEAm and BSTvl provide new anatomical insights into the functional organization of these limbic forebrain regions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s00429-012-0393-6

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Projections to the lateral hypothalamic area induce feeding behavior upon activation and projections from the NTS to the bed nucleus of the stria terminalis and the central amygdala are involved in anxiety as well as fear and avoidance behaviors, respectively.

    “projections to the lateral hypothalamic area induce feeding behavior upon activation and projections from the NTS to the bed nucleus of the stria terminalis, and the central amygdala are involved in anxiety as well as fear and avoidance behaviors, respectively (Bienkowski and Rinaman, 2013).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bienkowski and Rinaman, 2013

    Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 62

  1. Altschuler SM Bao X Bieger D Hopkins DA Miselis RR Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts J Comp Neurol 1989 283 2 248 268 2738198
  2. Bhatnagar S Dallman M Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress Neuroscience 1998 84 4 1025 1039 9578393
  3. Bhatnagar S Huber R Lazar E Pych L Vining C Chronic stress alters behavior in the conditioned defensive burying test: role of the posterior paraventricular thalamus Pharmacol Biochem Behav 2003 76 2 343 349 14592687
  4. Cecchi M Khoshbouei H Javors M Morilak DA Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress Neuroscience 2002 112 1 13 21 12044468
  5. Ciccocioppo R Fedeli A Economidou D Policani F Weiss F Massi M The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ J Neurosci 2003 23 28 9445 9451 14561874 PMC3035815
  6. Ciriello J Schultz CG Roder S Collateral axonal projections from ventrolateral medullary non-catecholaminergic neurons to central nucleus of the amygdala Brain Res 1994 663 2 346 351 7874522
  7. Ciriello J Solano-Flores LP Rosas-Arellano MP Kirouac GJ Babic T Medullary pathways mediating the parasubthalamic nucleus depressor response Am J Physiol Regul Integr Comp Physiol 2008 294 4 R1276 R1284 18287224
  8. Cullinan WE Herman JP Watson SJ Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis J Comp Neurol 1993 332 1 1 20 7685778
  9. Cullinan W Ziegler D Herman J Functional role of local GABAergic influences on the HPA axis Brain Struct Funct 2008 213 1 63 72 18696110
  10. de Olmos J Heimer L The concepts of the ventral striatopallidal system and extended amygdala Annals of the New York Academy of Sciences (Advancing from the Ventral Striatum to the Extended Amygdala: Implications for Neuropsychiatry and Drug Abuse) 1999 877 1 32 10415640
  11. DeVito JL Anderson ME Walsh KE A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta Exp Brain Res 1980 38 1 65 73 6766111
  12. Deyama S Nakagawa T Kaneko S Uehara T Minami M Involvement of the bed nucleus of the stria terminalis in the negative affective component of visceral and somatic pain in rats Behav Brain Res 2007 176 367 371 17101179
  13. Dong HW Swanson LW Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors J Comp Neurol 2003 463 4 434 472 12836178
  14. Dong HW Swanson LW Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis J Comp Neurol 2004 468 2 277 298 14648685
  15. Dong HW Swanson LW Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance J Comp Neurol 2006a 494 1 142 178 16304685 PMC2563961
  16. Dong HW Swanson LW Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses J Comp Neurol 2006b 494 1 75 107 16304681 PMC2707828
  17. Dong HW Petrovich GD Swanson LW Organization of projections from the juxtacapsular nucleus of the BST: a PHAL study in the rat Brain Res 2000 859 1 1 14 10720609
  18. Dong HW Petrovich GD Swanson LW Topography of projections from amygdala to bed nuclei of the stria terminalis Brain Res Rev 2001a 38 1–2 192 246 11750933
  19. Fanselow MS LeDoux JE Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala Neuron 1999 23 2 229 232 10399930
  20. Fendt M Endres T Apfelbach R Temporary inactivation of the bed nucleus of the stria terminalis but not of the amygdala blocks freezing induced by trimethylthiazoline, a component of fox feces J Neurosci 2003 23 1 23 28 12514197 PMC6742150
  21. Fisk GD Wyss JM Descending projections of infralimbic cortex that mediate stimulation-evoked changes in arterial pressure Brain Res 2000 859 1 83 95 10720617
  22. Freedman LJ Cassell MD Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat Brain Res 1994 633 1–2 243 252 7511034
  23. Funk CK O’Dell LE Crawford EF Koob GF Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats J Neurosci 2006 26 44 11324 11332 17079660 PMC6674550
  24. Gauriau C Bernard J-F Pain pathways and parabrachial circuits in the rat Exp Physiol 2002 87 02 251 258 11856971
  25. Gaykema RPA Chen C–C Goehler LE Organization of immune-responsive medullary projections to the bed nucleus of the stria terminalis, central amygdala, and paraventricular nucleus of the hypothalamus: evidence for parallel viscerosensory pathways in the rat brain Brain Res 2007 1130 130 145 17169348
  26. Geerling JC Loewy AD Aldosterone-sensitive neurons in the nucleus of the solitary tract: bidirectional connections with the central nucleus of the amygdala J Comp Neurol 2006 497 4 646 657 16739197 PMC2748794
  27. Goto M Swanson LW Axonal projections from the parasubthalamic nucleus J Comp Neurol 2004 469 4 581 607 14755537
  28. Harris GC Aston-Jones G Activation in extended amygdala corresponds to altered hedonic processing during protracted morphine withdrawal Behav Brain Res 2007 176 2 251 258 17123639 PMC1809796
  29. Heidbreder CA Groenewegen HJ The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics Neurosci Biobehav Rev 2003 27 6 555 579 14599436
  30. Jaferi A Nowak N Bhatnagar S Negative feedback functions in chronically stressed rats: role of the posterior paraventricular thalamus Physiol Behav 2003 78 3 365 373 12676271
  31. Jasnow AM Davis M Huhman KL Involvement of central amygdalar and bed nucleus of the stria terminalis corticotropin-releasing factor in behavioral responses to social defeat Behav Neurosci 2004 118 5 1052 1061 15506887
  32. Ju G Swanson LW Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: I. Cytoarchitecture J Comp Neurol 1989 280 4 587 602 2708568
  33. Ju G Swanson LW Simerly RB Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. Chemoarchitecture J Comp Neurol 1989 280 4 603 621 2468695
  34. Kalia M Sullivan JM Brainstem projections of sensory and motor components of the vagus nerve in the rat J Comp Neurol 1982 211 3 248 264 7174893
  35. Li S Kirouac GJ Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala J Comp Neurol 2008 506 2 263 287 18022956
  36. Myers EA Rinaman L Viscerosensory activation of noradrenergic inputs to the amygdala in rats Physiol Behav 2002 77 723 729 12527026
  37. Nagy FZ Pare D Timing of impulses from the central amygdala and bed nucleus of the stria terminalis to the brain stem J Neurophysiol 2008 100 6 3429 3436 18971295 PMC2604855
  38. Nakagawa T Yamamoto R Fujio M Suzuki Y Minami M Satoh M Kaneko S Involvement of the bed nucleus of the stria terminalis activated by the central nucleus of the amygdala in the negative affective component of morphine withdrawal in rats Neuroscience 2005 134 9 19 15939543
  39. Paxinos G Watson C The rat brain in stereotaxic coordinates 2007 6th edn. San Diego Elsevier Academic Press
  40. Radley JJ Sawchenko PE A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response J Neurosci 2011 31 26 9683 9695 21715634 PMC3197245
  41. Radley JJ Arias CM Sawchenko PE Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress J Neurosci 2006 26 50 12967 12976 17167086 PMC6674963
  42. Radley JJ Gosselink KL Sawchenko PE A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response J Neurosci 2009 29 22 7330 7340 19494154 PMC2743123
  43. Reilly S The parabrachial nucleus and conditioned taste aversion Brain Res Bull 1999 48 3 239 254 10229331
  44. Reynolds SM Zahm DS Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala J Neurosci 2005 25 50 11757 11767 16354934 PMC6726011
  45. Roder S Ciriello J Collateral axonal projections to limbic structures from ventrolateral medullary A1 noradrenergic neurons Brain Res 1994 638 1–2 182 188 7515319
  46. Sakai N Yamamoto T Role of the medial and lateral parabrachial nucleus in acquisition and retention of conditioned taste aversion in rats Behav Brain Res 1998 93 1–2 63 70 9659987
  47. Salazar-Jua´rez A Escobar C Aguilar-Roblero R Anterior paraventricular thalamus modulates light-induced phase shifts in circadian rhythmicity in rats Am J Physiol Regul Integr Comp Physiol 2002 283 4 R897 R904 12228059
  48. Santiago AC Shammah-Lagnado SJ Efferent connections of the nucleus of the lateral olfactory tract in the rat J Comp Neurol 2004 471 3 314 332 14991564
  49. Sesack SR Deutch AY Roth RH Bunney BS Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J Comp Neurol 1989 290 2 213 242 2592611
  50. Shammah-Lagnado SJ Alheid GF Heimer L Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat Neuroscience 1999 94 4 1097 1123 10625051
  51. Shammah-Lagnado SJ Alheid GF Heimer L Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat J Comp Neurol 2001 439 1 104 126 11584811
  52. Sun N Roberts L Cassell MD Rat central amygdaloid nucleus projections to the bed nucleus of the stria terminalis Brain Res Bull 1991 27 5 651 662 1721859
  53. Sved AF Cano G Card JP Neuroanatomical specificity of the circuits controlling sympathetic outflow to different targets Clin Exp Pharmacol Physiol 2001 28 1–2 115 119 11153526
  54. Swanson LW Cerebral hemisphere regulation of motivated behavior Brain Res 2000 886 1–2 113 164 11119693
  55. Swanson LW Brain maps: structure of the rat brain 2004 3rd edn. San Diego Elsevier
  56. Tanimoto S Nakagawa T Yamauchi Y Minami M Satoh M Differential contributions of the basolateral and central nuclei of the amygdala in the negative affective component of chemical somatic and visceral pain in rats Eur J Neurosci 2003 18 8 2343 2350 14622196
  57. Vertes RP Differential projections of the infralimbic and prelimbic cortex in the rat Synapse 2004 51 1 32 58 14579424
  58. Walker DL Davis M Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear J Neurosci 1997 17 23 9375 9383 9364083 PMC6573581
  59. Walker DL Toufexis DJ Davis M Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety Eur J Pharmacol 2003 463 1–3 199 216 12600711
  60. Walker DL Miles LA Davis M Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxietylike versus phasic fear-like responses Prog Neuropsychopharmacol Biol Psychiatry 2009 33 8 1291 1308 19595731 PMC2783512
  61. Watson RE Wiegand SJ Clough RW Hoffman GE Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology Peptides 1986 7 1 155 159 3520509
  62. Zardetto-Smith AM Beltz TG Johnson AK Role of the central nucleus of the amygdala and bed nucleus of the stria terminalis in experimentally-induced salt appetite Brain Res 1994 645 1–2 123 134 8062074

Cited by

Sorted by citations

Authors
Bienkowski, M. S., & Rinaman, L.
Affiliations
University of Pittsburgh (US)
Corresponding author
Rinaman, Linda
Venue
Brain Structure and Function
Published
2012-02-24
Volume
218
Issue
1
Pages
187-208
ISSN
  • 1863-2653 (ISSN-L)
  • 1863-2661
OpenAlex
W2091753010
Cited by
80
References
7
Citations by year
2026: 3 · 2025: 3 · 2024: 9 · 2023: 4 · 2022: 6 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 4 · 2017: 5 · 2016: 8 · 2015: 6 · 2014: 6 · 2013: 8 · 2012: 2
FWCI
3.61
Type
journal article
Language
en
Open access
Locations
  • Brain Structure and Function (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute for Health and Care Research
  • National Institutes of Health
  • National Institute of Mental Health (R01MH059911, MH-59911)
  • National Institute of Diabetes and Digestive and Kidney Diseases (T32DK063922, DK 063922)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
central extended amygdala, limbic forebrain, stress response, fear and anxiety, social defeat
MeSH terms
Amygdala, Animals, Cholera Toxin, Iontophoresis, Male, Neural Pathways, Neurons, Septal Nuclei, Stilbamidines, Rats, Sprague-Dawley, Rats, Neuronal Tract-Tracers, Neuroanatomical Tract-Tracing Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review