Cholinergic projections to the basolateral amygdala: A combined Evans Blue and acetylcholinesterase analysis
Abstract
The origins and acetylcholinesterase (AChE, EC 3.1.1.7) content of neurons projecting to the AChE-rich basolateral amygdala were studied by infusing Evans Blue (EB), a retrogradely transported fluorescent label, into that neural region and, following microscopic evaluation of labelled somata, staining the same tissue sections for AChE according to the pharmacohistochemical regimen. The following basal forebrain areas contained cells labelled with EB: the lateral preoptic area, ventral pallidum, nuclei of the diagonal band, medial septal nucleus, bed nucleus of the stria terminalis, and substantia innominata. The majority of the basal forebrain neurons projecting to the basolateral amygdala stained intensely for AChE, suggesting that they were cholinergic. In the brainstem, EB-labelled neurons staining intensely for AChE were found less frequently, but a few were observed in the nucleus tegmenti pendunculopontis, locus ceruleus, subcerulear region, and reticular formation. Cells accumulating EB after basolateral amygdala infusion but demonstrating no, weak, or moderate AChE activity were seen in the orbitofrontal, anterior cingulate, temporal, and insular cortices; the mediodorsal, paraventricular, and parataenial nuclei of the thalamus; the periventricular gray substance; the ventromedial mesencephalic tegmentum; the lateral and compact portions of the substantia nigra; the dorsal raphe; the dorsal tegmental nucleus; and the dorsal parabrachial nucleus. On the basis of staining intensity, intracellular organization of the AChE reaction product, and previous results in the literature, we conclude that the major cholinergic input to the basolateral amygdala derives from the basal forebrain.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
The nucleus basalis of Meynert projects to the amygdala and is the primary source of cholinergic input to the basolateral amygdala.
“Furthermore, NBM projects to the amygdala and is the primary source of cholinergic input to the basolateral amygdala (44,46,56,57).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [56]
Cites
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,143 · see citing works
A stereotaxic atlas of the rat brain
Pellegrino, L. J., & Cushman, A. J. (1967) · Plenum Press eBooks · Cited by 4,695 · see citing works
A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES
Karnovsky, M. J., & ROOTS, L. (1964) · Journal of Histochemistry & Cytochemistry · doi:10.1177/12.3.219 · Cited by 3,389 · see citing works
A stereotaxic atlas of the rat brain
Brodal, P. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90013-5 · Cited by 2,799 · see citing works
Steinbusch, H. W. M. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90146-9 · Cited by 2,415 · see citing works
Krettek, J. E., & Price, J. L. (1978) · Journal of Comparative Neurology · doi:10.1002/cne.901780204 · Cited by 1,293 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
A Histochemical Method for Localizing Cholinesterase Activity.
Koelle, G. B., & Friedenwald, J. S. (1949) · Experimental Biology and Medicine · doi:10.3181/00379727-70-17013 · Cited by 1,192 · see citing works
THE ASCENDING CHOLINERGIC RETICULAR SYSTEM: NEOCORTICAL, OLFACTORY AND SUBCORTICAL PROJECTIONS
Shute, C. C. D., & Lewis, P. R. (1967) · Brain · doi:10.1093/brain/90.3.497 · Cited by 1,120 · see citing works
Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas
Krieg, W. J. S. (1946) · The Journal of Comparative Neurology · doi:10.1002/cne.900840205 · Cited by 1,018 · see citing works
The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat
Kimura, H., McGeer, P. L., Peng, J. H., & McGeer, E. G. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.902000202 · Cited by 966 · see citing works
The biology of cholinesterases
Silver, A. (1974) · Medical Entomology and Zoology · Cited by 890 · see citing works
Taste pathways to hypothalamus and amygdala
Norgren, R. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901660103 · Cited by 761 · see citing works
Krettek, J. E., & Price, J. L. (1978) · Journal of Comparative Neurology · doi:10.1002/cne.901780205 · Cited by 727 · see citing works
Lehmann, J. C., Nagy, J. I., Atmadja, S., & Fibiger, H. C. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90195-5 · Cited by 619 · see citing works
A Stereotaxic Atlas of the Developing Rat Brain
Sherwood, N. M., & Timiras, P. S. (1970) · Medical Entomology and Zoology · Cited by 588 · see citing works
An autoradiographic study of the efferent connections of the preoptic region in the rat
Swanson, L. W. (1976) · Journal of Comparative Neurology · doi:10.1002/cne.901670207 · Cited by 588 · see citing works
A radioautographic study of the efferent pathways of the nucleus locus coeruleus
Pickel, V. M., Segal, M., & Bloom, F. E. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901550103 · Cited by 510 · see citing works
Swezy, O. (1928) · Science · doi:10.1126/science.68.1751.60 · Cited by 461 · see citing works
Cholinergic projections from magnocellular nuclei of the basal forebrain to cortical areas in rats
Wenk, H., Bigl, V., & Meyer, U. (1980) · Brain Research Reviews · doi:10.1016/0165-0173(80)90011-9 · Cited by 445 · see citing works
Jones, E. G., Burton, H., Saper, C. B., & Swanson, L. W. (1976) · Journal of Comparative Neurology · doi:10.1002/cne.901670402 · Cited by 420 · see citing works
Fibre Degeneration Following Lesions of the Amygdaloid Complex in the Monkey
Nauta, W. J. H. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-7920-1_12 · Cited by 373 · see citing works
Afferent connections to the amygdaloid complex of the rat and cat. I. Projections from the thalamus
Ottersen, O. P., & Ben‐Ari, Y. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870209 · Cited by 303 · see citing works
Temporal neocortical afferent connections to the amygdala in the rhesus monkey
Herzog, A. G., & Hoesen, G. W. V. (1976) · Brain Research · doi:10.1016/0006-8993(76)90822-2 · Cited by 294 · see citing works
Subcortical afferents of the amygdaloid complex in the rat: an HRP study
Veening, J. G. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90121-0 · Cited by 237 · see citing works
NEURAL ASSOCIATIONS OF THE AMYGDALOID COMPLEX IN THE MONKEY
NAUTA, W. J. H. (1962) · Brain · doi:10.1093/brain/85.3.505 · Cited by 231 · see citing works
Woolf, N. J., & Butcher, L. L. (1981) · Brain Research Bulletin · doi:10.1016/0361-9230(81)90004-6 · Cited by 221 · see citing works
Self-citationOttersen, O. P. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901940113 · Cited by 218 · see citing works
The fibre-connections of the forebrain
Knook, H. L. (1965) · Davis eBooks · Cited by 140 · see citing works
Cholinergic projections from the basal forebrain of rat to the amygdala
Nagai, T., Kimura, H., Maeda, T., McGeer, P., Peng, F., & McGeer, E. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-04-00513.1982 · Cited by 140 · see citing works
The amygdaloid nucleus in the rat
Brodal, A. (1947) · The Journal of Comparative Neurology · doi:10.1002/cne.900870102 · Cited by 138 · see citing works
Ben‐Ari, Y., Zigmond, R. E., Shute, C. C. D., & Lewis, P. R. (1977) · Brain Research · doi:10.1016/0006-8993(77)90397-3 · Cited by 133 · see citing works
The corpus striatum of the rat. Studies on the brain of the rat. No. 3
GURDJIAN, E. S. (1928) · The Journal of Comparative Neurology · doi:10.1002/cne.900450110 · Cited by 119 · see citing works
A cingulo-amygdaloid projection in the rhesus monkey
Pandya, D. Ν., Hoesen, G. W. V., & Domesick, V. B. (1973) · Brain Research · doi:10.1016/0006-8993(73)90540-4 · Cited by 117 · see citing works
Efferent connections of the orbitofrontal cortex in the marmoset(Saguinus oedipus)
Leichnetz, G. R., & Astruc, J. A. (1975) · Brain Research · doi:10.1016/0006-8993(75)90973-7 · Cited by 116 · see citing works
Butcher, L. L., Eastgate, S. M., & Hodge, G. K. (1974) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00499527 · Cited by 111 · see citing works
Self-citationEmson, P. C., Paxinos, G., Salle, G. L. G. L., Ben‐Ari, Y., & Silver, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90559-6 · Cited by 110 · see citing works
Hoover, D. B., & Jacobowitz, D. M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90944-2 · Cited by 108 · see citing works
Parent, A., & Butcher, L. L. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901700206 · Cited by 103 · see citing works
Self-citationBen‐Ari, Y., Zigmond, R. E., & Moore, K. E. (1975) · Brain Research · doi:10.1016/0006-8993(75)90786-6 · Cited by 94 · see citing works
Siegel, A., Fukushima, T., Meibach, R. C., Burke, L., Edinger, H. M., & Weiner, S. (1977) · Brain Research · doi:10.1016/0006-8993(77)91048-4 · Cited by 94 · see citing works
Dopamine evoked inhibition of single cells of the feline putamen and basolateral amygdala.
Ben‐Ari, Y., & Kelly, J. S. (1976) · The Journal of Physiology · doi:10.1113/jphysiol.1976.sp011308 · Cited by 91 · see citing works
SOME CONNECTIONS OF THE ORBITO-FRONTO-TEMPORAL, LIMBIC AND HIPPOCAMPAL AREAS OF MACACA MULATTA
Pribram, K. H., Lennox, M. A., & Dunsmore, R. H. (1950) · Journal of Neurophysiology · doi:10.1152/jn.1950.13.2.127 · Cited by 90 · see citing works
Inputs and Outputs of the Amygdala: What the Amygdala is Trying to Tell the Rest of the Brain
GLOOR, P. (1978) · Springer eBooks · doi:10.1007/978-1-4757-0716-8_8 · Cited by 81 · see citing works
Acetylcholinesterase and catecholamine distribution in the locus ceruleus of the rat
Albanese, A., & Butcher, L. L. (1980) · Brain Research Bulletin · doi:10.1016/0361-9230(80)90184-7 · Cited by 63 · see citing works
Self-citationButcher, L. L., & Marchand, R. (1978) · European Journal of Pharmacology · doi:10.1016/0014-2999(78)90301-1 · Cited by 62 · see citing works
Self-citationEfferent connections of the basal and lateral nuclei of the amygdala in the cat
Hall, E. (1963) · American Journal of Anatomy · doi:10.1002/aja.1001130110 · Cited by 60 · see citing works
Butcher, L. L., & Woolf, N. J. (1982) · Progress in brain research · doi:10.1016/s0079-6123(08)64188-6 · Cited by 58 · see citing works
Self-citationDistribution of acetylcholinesterase and monoamine oxidase in the amygdala of the guinea pig
Hall, E., & Geneser-Jensen, F. A. (1971) · Cell and Tissue Research · doi:10.1007/bf00335536 · Cited by 47 · see citing works
Parent, A., & O'Reilly-Fromentin, J. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90045-4 · Cited by 36 · see citing works
Butcher, L. L., Marchand, R., Parent, A., et al. (1977) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(77)90232-5 · Cited by 33 · see citing works
Self-citationStudies on the forebrain of the mouse. Golgi observations.
Valverde, F. (1963) · Europe PMC (PubMed Central) · Cited by 31 · see citing works
Nigro‐amygdaloid fiber connections in the cat
Kaelber, W. W., & Afifi, A. K. (1977) · American Journal of Anatomy · doi:10.1002/aja.1001480110 · Cited by 14 · see citing works
Kosmal, A. (1976) · PubMed · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mesulam, M. ‐., Mufson, E. J., Levey, A. I., & Wainer, B. H. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902140206 · Cited by 1,962 · see citing works
Alheid, G. F., & Heimer, L. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90217-5 · Cited by 1,217 · see citing works
Cholinergic systems in mammalian brain and spinal cord
WOOLF, N. (1991) · Progress in Neurobiology · doi:10.1016/0301-0082(91)90006-m · Cited by 948 · see citing works
Self-citationRye, D. B., Wainer, B. H., Mesulam, M.-M., Mufson, E. J., & Saper, C. B. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90083-6 · Cited by 743 · see citing works
Piecing together the Puzzle of Basal Forebrain Anatomy
Heimer, L., & Alheid, G. F. (1991) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4757-0145-6_1 · Cited by 310 · see citing works
Amygdala Modulation of Memory Consolidation: Interaction with Other Brain Systems
McGaugh, J. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4082 · Cited by 279 · see citing works
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“Furthermore, NBM projects to the amygdala and is the primary source of cholinergic input to the basolateral amygdala (44,46,56,57).”
BackgroundPostnatal development of cholinergic neurons in the rat: I. Forebrain
Gould, E., Woolf, N. J., & Butcher, L. L. (1991) · Brain Research Bulletin · doi:10.1016/0361-9230(91)90209-3 · Cited by 135 · see citing works
Self-citationPeña, C. J., Neugut, Y. D., Calarco, C. A., & Champagne, F. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12479 · Cited by 120 · see citing works
Cholinergic activation of the basolateral amygdala regulates unlearned freezing behavior in rats
Power, A. E., & McGaugh, J. L. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00046-3 · Cited by 65 · see citing works
Power, A. E., & McGaugh, J. L. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4030 · Cited by 57 · see citing works
Houser, C. R. (1990) · Journal of Electron Microscopy Technique · doi:10.1002/jemt.1060150103 · Cited by 55 · see citing works
Effects of feeding and insulin on extracellular acetylcholine in the amygdala of freely moving rats
Hajnal, A., Pothos, E. N., Lénárd, L., & Hoebel, B. G. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01291-2 · Cited by 39 · see citing works
Van der Zee, E. A., Roozendaal, B., Bohus, B., Koolhaas, J. M., & Luiten, P. G. M. (1996) · Neuroscience · doi:10.1016/s0306-4522(96)00359-4 · Cited by 34 · see citing works
- Authors
- Woolf, N. J., & Butcher, L. L.
- Affiliations
- University of California, Los Angeles (US)
- Venue
- Brain Research Bulletin
- Publisher
- Elsevier BV
- Published
- 1982-06
- Volume
- 8
- Issue
- 6
- Pages
- 751-763
- ISSN
- 0361-9230 (ISSN-L)
- OpenAlex
- W2002049010
- Cited by
- 231
- References
- 54
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 9 · 2022: 4 · 2021: 5 · 2020: 4 · 2019: 2 · 2018: 4 · 2017: 2 · 2016: 7 · 2014: 4 · 2013: 2 · 2012: 2
- FWCI
- 8.83
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Pharmacology › Cholinesterase and Neurodegenerative Diseases
- Keywords
- cholinergic projections, basolateral amygdala, acetylcholinesterase, cholinergic neurons, basal forebrain, lateral preoptic area, ventral pallidum, diagonal band, medial septum, bed nucleus of the stria terminalis, substantia innominata, retrograde tracing, Evans blue
- MeSH terms
- Acetylcholinesterase, Amygdala, Animals, Axonal Transport, Brain, Efferent Pathways, Evans Blue, Female, Neurons, Rats, Inbred Strains, Rats
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
