The Amygdalostriatal Projection

An Analysis of Synaptic Inputs to GABAergic Interneuron Subtypes
  • Abbas F. Sadikot
  • Teresa M. Rudkin
  • Yoland Smith
Part of the Advances in Behavioral Biology book series (ABBI, volume 47)


The striatum receives massive inputs from the cortex, thalamus and midbrain, and is also afferented by serotoninergic and noradrenergic cells groups, and the globus pallidus (Heimer et al. 1995; Parent, 1990, for reviews). Recent studies have revealed a dense amygdalostriatal projection which is centered upon the nucleus accumbens, but which tographically distributes over a large striatal area excluding the sensorimotor sector (Wright and Groenewegen, 1995; Johnson et al., 1994a,b; McDonald et al, 1991; Kita and Kitai, 1990; Russchen and Price, 1984; Groenewegen et al, 1982, 1980; Kelley et al., 1982; DeFrance et al., 1980; Krettek and Price,1978; Dafny et al. 1975; de Olmos, 1972). In rodents, the amygdalostriatal projection arises mainly from the basolateral nuclear complex. Other amygdala nuclei contributing to the projection include the accessory basal and cortical nuclei, the amygdalohippocampal transitional area, and the nucleus of the lateral olfactory tract. These inputs are excitatory and use glutamate as a neurotransmitter (Callaway et al., 1991; Robinson and Beart, 1988; Christie et al, 1987; Fuller et al., 1987). As is true for cortical projections to the dorsal and ventral striatum (Sesack and Pickel, 1992; Totterdell and Smith, 1989; Dubé et al, 1988; Frotscher et al.,’ 81; Somogyi et al,’ 81; Kemp and Powell,’ 71), amygdala projections terminate mainly on dendritic spines of medium spiny neurons (Johnson et al., 1994a,b; Kita and Kitai, 1990).


Nucleus Accumbens Dendritic Spine Projection Neuron Ventral Striatum Medium Spiny Neuron 
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  1. Bennett, B.D. and Bolam, J.P., 1994, Synaptic input and output of parvalbumin-immunoneractive neurons in the neostriatum of the rat. Neuroscience 62: 707–719.PubMedCrossRefGoogle Scholar
  2. Bennett, B.D. and Bolam, J.P., 1993, Characterization of calretinin-immunoreactive structures in the striatum of the rat. Brain Res. 609: 137–148.PubMedCrossRefGoogle Scholar
  3. Bolam, J.P., Powell, J.F., Wu, J.Y., and Smith, A.D., 1985, GAD-immunoreactive structures in the rat neostriatum: a study including combination of Golgi-impregnation with immunocytochemistry. J. Comp. Neurol. 237: 1–20.PubMedCrossRefGoogle Scholar
  4. Bolam, J.P., Clark, D.J., Smith A.D., and Somogyi, P., 1983, A type of aspiny neuron in the rat neostriatum accumulates (3H-)GABA: Combination of Golgi-staining, autoradiography and electron microscopy. J. Comp Neurol. 213: 121–134.PubMedCrossRefGoogle Scholar
  5. Callaway, C.W., Hakan, R.L., and Henriksen, S.J., 1991, Distribution of amygdala input to the nucleus accumbens septi-an electrophysiological investigation. J Neural Trans.-Gen. Section. 83: 215–225.CrossRefGoogle Scholar
  6. Christie, M.J., Summers, R.J., Stephenson, J.A., Cook, C.J., Beart, P.M., 1987, Excitatory amino acid projections to the nucleus accumbens septi in the rat: a retrograde transport study utilizing D(3H)aspartate and (3H)GABA. Neuroscience. 22: 425–439.PubMedCrossRefGoogle Scholar
  7. Cowan, R.L., Wilson, C.J., Emson, P.C., and Heinzmann, C.W., 1990, Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. Comp. Neurol. 302: 197–205.PubMedCrossRefGoogle Scholar
  8. Dafny, N., Dauth, G., and Gilman, S., 1975, A direct input from the amygdaloid complex to the caudate nucleus of the rat. Exp. Brain Res. 23:203–210.PubMedCrossRefGoogle Scholar
  9. De Olmos, J.S., 1972,. The amygdaloid projection field in the rat as studied with the cupric silver method. In “The Neurobiology of the Amygdala” (B.E. Eleftheriou, Ed.), pp. 145–204. Plenum, New York.CrossRefGoogle Scholar
  10. De France, J.F., Marchand, J.E., Stanley, J.C., Sikes, R.W., and Chronister, R.B., 1980, Convergence of excitatory amygdaloid and hippocampal input in the nucleus accumbens septi. Brain Res. 185: 183–186.CrossRefGoogle Scholar
  11. Dubé, L., Smith, A.D., Bolam, J.P., 1988, Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium spiny neurons in the rat neostriatum. J. Comp. Neurol. 267: 455–471.PubMedCrossRefGoogle Scholar
  12. Frotscher, M., Rinne, U., Hassler, R., and Wagner. A., 1981, Termination of cortical afferents on identified neurons in the caudate nucleus of the cat: A combined Golgi-EM degeneration study. Exp. Brain Res. 41: 329–337.PubMedGoogle Scholar
  13. Fuller, T.A., Russchen, F. T., and Price, J.L., 1987, Sources of presumptive glutamatergic/aspartergic afferents to the rat ventral striatopallidal region. J. Comp. Neurol. 258: 317–338.PubMedCrossRefGoogle Scholar
  14. Geneser-Jensen, F.A., and Blackstad, T.W., 1971, Distribution of acetylcholinesterase in the hippocampus and regions of the globus pallidus I. Entorhinal area, parasubiculum and presubiculum. Z Zeilforsch Mekrosh Anat. 144:460–481.CrossRefGoogle Scholar
  15. Groenewegen, H.J., Berendse, H.W., Meredith, G.E., Haber, S.N., Voorn, P., Wolters, J.G., and Lohman, A.H.M., 1991, Functional anatomy of the ventral, limbic system-innervated striatum. In: The Mesolimbic Dopamine System: From Motivation to Action (P. Willner and J. Scheel-Kruger, Eds.). Wiley, Chichester, United Kingdom, pp. 16–90.Google Scholar
  16. Groenewegen, H.J., Room, P, Witter, M.P., and Lohman A.H., 1982, Cortical afferents of the nucleus accumbens in the cat, studied with anterograde and retrograde transport techniques. Neuroscience. 7: 977–996.PubMedCrossRefGoogle Scholar
  17. Groenewegan, H.J., Room, P., Witter, M.P., and Lohman, A.H.M., 1980, Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid, Neuroscience. 5: 1903–1916.CrossRefGoogle Scholar
  18. Groves, P.M, 1983, A theory of the functional organization of the striatum and the neostriatal control of voluntary movement. Brain Res Rev. 5: 109–132.CrossRefGoogle Scholar
  19. Heimer, L., Zahm, D.S., and Alheid, G.F. (1995) Basal Ganglia. In: The Rat Nervous System (G. Paxinos, Ed.), Academic Press, San Diego. pp.579–628.Google Scholar
  20. Jaeger, D., Kita, H., and Wilson, C.J., 1994, Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J. Neurophysiol. 72: 2555–2558.PubMedGoogle Scholar
  21. Johnson, L.R., Aylward, R.L.M., and Totterdell, S., 1994a, Synaptic organization of the amygdalar input to the nucleus accumbens of the rat. In: The Basal Ganglia IV. New Ideas and Data on Structure and Function G. Percheron, J.S. McKenzie and JS Feger, Eds., Plenum Press, New York, pp 109–114.CrossRefGoogle Scholar
  22. Johnson, L.R., Aylward, R.L.M., Hussain, Z., and Totterdell, S., 1994b, Input from the amygdala to the ratnucleus accubens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience 61: 851–865.PubMedCrossRefGoogle Scholar
  23. Kawaguchi, Y., 1993, Physiological, morphological, and histochemical characterization of 3 classes of interneurons in the rat neostriatum. J. Neurosci. 13: 4908–4923.PubMedGoogle Scholar
  24. Kelley, A.E., Domesick, V.B., and Nauta, W.J.H., 1982, The amygdalostriatal projection in the rat-An anatomical study by anterograde and retrograde tracing methods. Neuroscience. 7: 615–630.PubMedCrossRefGoogle Scholar
  25. Kemp J. and Powell, T.P.S., 1971, The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: a study with the Golgi-method. Phil. Trans. R. Soc. Lond. B. 262: 429–439.CrossRefGoogle Scholar
  26. Kita, H., 1993, GABAergic circuts of the striatum. In: Progress in Brain Research, Vol. 99, (G.W. Arbuthnott, and P.C. Emson eds.), Elsevier, Amsterdam, pp. 51–72.Google Scholar
  27. Kita, H. and Kitai, S.T., 1990, Amygdaloid projections to the frontal cortex and the striatum in the rat. J. Comp. Neurol. 298: 40–49.PubMedCrossRefGoogle Scholar
  28. Kita, H., Kosaka, T., and Heizmann, C.W., 1990, Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res. 536: 1–15.PubMedCrossRefGoogle Scholar
  29. Kita, H. and Kitai, S.T., 1988, GAD-immunoreactive neurons in the rat neostriatum: their morphological types and populations. Brain Res. 447: 346–352.PubMedCrossRefGoogle Scholar
  30. Krettek, J.E. and Price, J.L., 1978, Amygdaloid projection to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp.Neurol. 178: 225–254.PubMedCrossRefGoogle Scholar
  31. Kubota, Y., Mikawa, S., and Kawaguchi, Y., 1993, Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. Neuroreport. 5: 205–208.PubMedCrossRefGoogle Scholar
  32. Lapper, S.R., Smith, Y, Sadikot, A.F., Parent, A., and Bolam, J.P., 1992, Cortical input to parvalbumin-immunoreactive neurons in the putamen of the squirrel monkey. Brain Res. 580: 215–224.PubMedCrossRefGoogle Scholar
  33. Llewellyn-Smith, I.J., Pilowsky, P., and Minson, J.B., 1993, The tungstate-stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons. J. Neurosci. Methods. 46: 27–40.PubMedCrossRefGoogle Scholar
  34. MacDonald, A.J., 1994, Calretinin immunoreactive neurons in the basolateral amygdala of the rat and monkey. Brain Res. 667: 238–242.CrossRefGoogle Scholar
  35. McDonald, A.J., 1991, Topographic organization of amygdaloid projections to the caudate putamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience. 44: 15–33.PubMedCrossRefGoogle Scholar
  36. McGeorge, A.J., and Faull, R.L.M., 1989, The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience. 29: 503–537.PubMedCrossRefGoogle Scholar
  37. Parent, A., 1990, Extrinsic connections of the basal ganglia. Trends in Neurosci. 13: 254–25CrossRefGoogle Scholar
  38. Pennartz, C.M.A., and Kitai, S.T., 1991, Hippocampal inputs to identified neurons in an in vitro slice preparation of the rat nucleus accumbens-evidence for feed-forward inhibition. J. Neurosci. 11: 2838–2847.PubMedGoogle Scholar
  39. Robinson, T.G. and Beart, P.M., 1988, Excitant projections from the rat amygdala and thalamus to the nucleus accumbens. Brain Res. Bull. 20: 467–471.PubMedCrossRefGoogle Scholar
  40. Russchen, F.T. and Price, J.L., 1984, Amygdalostriatal projections in the rat: Topographical organization and fibre morphology shown using lectin PHA-L as an anterograde tracer. Neurosci. Lett. 47: 15–22.PubMedCrossRefGoogle Scholar
  41. Sesack, S.R., and Pickel, V.M., 1992, Prefrontal cortical afferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 320: 145–160.PubMedCrossRefGoogle Scholar
  42. Smith, A.D., and Bolam, J.P., 1990, The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci. 13: 259–265.PubMedCrossRefGoogle Scholar
  43. Smith, Y., and Bolam, J.P., 1992, Combined approaches to experimental neuroanatomy: combined tracing and immunocytochemical techniques for the study of neuronal microcircuits, Experimental Neuroanatomy: A Practical Approach, J.P. Bolam, ed. Oxford University Press, Oxford, pp.239–266.Google Scholar
  44. Somogyi, P., Bolam, J.P., and Smith, A.D., 1981, Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J. Comp. Neurol. 195: 567–584.PubMedCrossRefGoogle Scholar
  45. Totterdell, S., and Smith, A.D., 1989, Convergence of hippocampal dopminergic input onto identified neurons in the nucleus accumbens of the rat. J. Chem. Neuroanat. 2: 285–298.PubMedGoogle Scholar
  46. Wilson, C.J, Chang, H.T., and Kitai, S.T, 1990, Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J.Neurosci. 10: 508–519.PubMedGoogle Scholar
  47. Wouterlood, F.G., Bol, J.G.J.N., and Steinbusch, H.W.M., 1987, Double-label immunocytochemistry: Combination of anterograde neuroanatomical tracing with Phaseolus vulgaris-leucoglutinin and enzyme histochemistry of target neurons. J. Histochem. Cytochem. 35: 815–823.CrossRefGoogle Scholar
  48. Wright, C.I. and Groenewegen, H.J., 1995, Patterns of convergence and segregation in the medial nucleus accumbens of the rat: relationships of prefrontal cortical, midline thalamic, and basal amygdaloid afferents. J. Comp. Neurol. 361: 383–403.PubMedCrossRefGoogle Scholar
  49. Zahm, D.S. and Heimer, L., 1992, Specificity in the efferent projections of the nucleus accumbens in the rat: Comparison of the rostral pole projection patterns with those of the core and shell. J. Comp. Neurol. 327:220–232.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Abbas F. Sadikot
    • 1
  • Teresa M. Rudkin
    • 1
  • Yoland Smith
    • 2
  1. 1.Division of Neurosurgery, Department of Neurology and Neurosurgery, Montreal Neurological Institute, Faculy of MedicineMcGill UniversityMontrealCanada
  2. 2.Centre de Recherche en Neurobiologie, Enfant-Jésus Hospital, Faculty of MedicineLaval UniversityQuebecCanada

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