Amygdala afferents monosynaptically innervate corticospinal neurons in rat medial prefrontal cortex

Journal of Comparative Neurology

Volumn 520, Issue 11, 2012, Pages 2440-2458

  Gabbott, Paul ^a,b,c   Warner, Tracy Ann ^a   Brown, Jacki ^b   Salway, Philip ^a   Gabbott, Thomas ^c   Busby, Sarah ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b OPEN UNIVERSITY   (United Kingdom)

^c Neural Architectonics Centre   (United Kingdom)

Author keywords

Amygdalocortical afferents; Infralimbic, prelimbic, and anterior cingulate cortices; Pyramidal neurons; Subcortical autonomic target regions

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; INNERVATION; MALE; MEDIAL PREFRONTAL CORTEX; NONHUMAN; PERIKARYON; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SENSORY NERVE; SYNAPSE;

AFFERENT PATHWAYS; AMYGDALA; ANIMALS; MALE; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS, AFFERENT; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84860904261     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23047     Document Type: Article

References (77)

1. Aggleton JP, ed. 2000. The amygdala. A functional analysis. 2nd ed. Oxford: Oxford University Press.
2. Akintunde A, Buxton DF. 1992. Origins and collateralization of corticospinal, corticopontine, corticorubral and corticostriatal tracts: a multiple retrograde fluorescent tracing study. Brain Res 586: 208-218.
3. Bacon SJ, Smith AD. 1993. A monosynaptic pathway from an identified vasomotor centre in the medial prefrontal cortex to an autonomic area in the thoracic spinal cord. Neuroscience 54: 719-728.
4. Bacon SJ, Headlam AJN, Gabbott PLA, Smith AD. 1996. Amygdala input to medial prefrontal cortex (mPFC) in the rat: a light and electron microscope study. Brain Res 720: 211-219.
5. Bolam JP, ed. 1992. Experimental neuroanatomy. A practical approach. Oxford: IRL Press of Oxford University Press.
6. Buhl EH, L̈bke J. 1989. Intracellular lucifer yellow injection in fixed brain slices combined with retrograde tracing, light and electron microscopy. Neuroscience 28: 3-16.
7. Cassell MD, Chittick CA, Siegel MA, Wright DJ. 1989. Collateralization of the amygdaloid projections of the rat prelimbic and infralimbic cortices. J Comp Neurol 279: 235-248.
8. Catsman-Berrevoets CE, Kuypers HGJM. 1981. A search for corticospinal collaterals to thalamus and mesencephalon by means of multiple retrograde fluorescent tracers in cat and rat. Brain Res 218: 15-33.
9. Cechetto DF, Saper 1990. Role of the cerebral cortex in autonomic function. In Loewy AD, Spyer KM, editors. Central regulation of autonomic function. New York: Oxford University Press. p 208-223.
10. Chudasama Y, Robbins TW. 2003. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 24: 8771-8780.
11. Dalley JW, Cardinal RN, Robbins TW. 2004. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28: 771-784.
12. DeFelipe J. 1997. Types of neurones, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14: 1-19.
13. DeFelipe J, Fairen A. 1982. A type of basket cell in superficial layers of the cat visual cortex. A Golgi electron microscope study. Brain Res 244: 9-16.
14. DeFelipe J, Fairen A. 1993. A simple and reliable method for correlative light and electron microscopic studies. J Histochem Cytochem 41: 769-772.
15. Deschênes MA, Landry P. 1979. Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Res 178: 251-274.
16. Ferino F, Thierry AN, Saffroy M, Glowinski J. 1987. Interhemispheric and subcortical collaterals of medial prefrontal cortical neurones in the rat. Brain Res 417: 257-266.
17. Gabbott PLA, Martin KAC, Whitteridge D. 1987. Connections between pyramidal neurones in layer 5 of cat visual cortex (area 17). J Comp Neurol 259: 364-381.
18. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ. 1997. Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J Comp Neurol 377: 465-499.
19. Gabbott P, Headlam A, Busby S. 2002. Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurone and NADPH-diaphorase reactive cells in the medial prefrontal cortex (areas 25/32) of the rat. Brain Res 946: 314-322.
20. Gabbott PL, Warner TA, Jays PR, Bacon SJ. 2003. Areal and synaptic connectivity of prelimibic (area 32) infralimbic (area 25) and the insular cortices in the rat. Brain Res 893: 59-71.
21. Gabbott PL, Warner T, Busby SJ. 2007. Catecholaminergic neurons in meduallary nuclei are among the post-synaptic targets of descending projections from infralimbic area 25 of the rat medial prefrontal cortex. Neuroscience 144: 623-635.
22. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ. 2005. Prefrontal cortex in the rat: projections to subcortical autonomic, motor and limbic centres. J Comp Neurol 492: 145-177.
23. Gabbott PL, Warner TA, Busby SJ. 2006. Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex. Neurosci 139: 1039-1048.
24. Garcia R, Vouimba RM, Baudry M, Thompson RF. 1999. The amygdala modulates prefrontal cortex activity relative to conditioned fear. Nature 402: 294-296.
25. Gerfen CR, Sawchenko PE. 1984. A method for anterograde axonal tracing of chemically specified circuits in the central nervous system: combined Phaseolus vulgaris-leucoagglutinin (PHA-L) tract-tracing and immunohistochemistry. Brain Res 343: 144-150.
26. González-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. 2005. Functional properties of fast spiking interneurones and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953.
27. Gray EG. 1959. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 24: 420-433.
28. Groenewegen HJ, Uylings HBM. 2000. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126: 3-28.
29. Hardy SGP. 1994. Anatomical data supporting the concept of prefrontal influences upon hypothalamomedullary relays in the rat. Neurosci Lett 169: 17-20.
30. Harrison LM, Mair RG. 1996. A comparison of the effects of frontal cortical and thalamic lesions on measures of spatial learning and memory in the rat. Behav Brain 75: 195-206.
31. Heidbreder CA, Groenewegen HJ. 2003. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev 27: 555-579.
32. Holstege G, Bandler R, Saper CB. 1996. The emotional motor system. Progress in brain research, vol 107. Amsterdam: Elsevier.
33. Hurley KM, Herbert H, Moga MM, Saper CB. 1991. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308: 249-276.
34. Hussain Z, Johnson LR, Totterdell S. 1996. A light and electron microscopic study of NADPH diaphorase calretinin- and parvalbumin-containing neurons in the rat nucleus accumbens. J Chem Neuroanat 10: 19-39.
35. Kawaguchi Y. 1993. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416-431.
36. Kawaguchi Y. 2001. Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci 21: 7261-7272.
37. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31: 277-287.
38. Kawaguchi Y, Kubota Y. 1993. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindin D28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396.
39. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex 7: 476-486.
40. Kesner RP, Ragozzino ME. 2003. The role of the prefrontal cortex in object-place learning: a test of the attribute specificity model. Behav Brain Res 146: 159-165.
41. Kita H, Kitai ST 1990. Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol 298: 40-49.
42. Krettek JE, Price JL 1977. Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J Comp Neurol 172: 687-722.
43. Kuroda M, Murakami K, Kishi K, Price JL. 1995. Thalamocortical synapses between axons from the mediodorsal thalamic nucleus and pyramidal cells in the prelimbic cortex of the rat. J Comp Neurol 356: 143-151.
44. Landry P, Labele A, Deschênes M. 1980. Intracortical distribution of axonal collaterals of pyramidal tract cells in the cat motor cortex. Brain Res 191: 327-336.
45. Landry P, Wilson CJ, Kitai ST. 1984. Morphological and electrophysiological characteristics of pyramidal tract neurons in the rat. Exp Brain Res 57: 177-190.
46. Levesque M, Charara A, Cagnon S, Parent A. 1996. Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res 709: 311-315.
47. Loewy AD. 1991. Forebrain nuclei involved in autonomic control. Prog Brain Res 87: 253-268.
48. Maroun M, Richter-Levin G. 2003. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23: 4406-4409.
49. McDonald AJ. 1991. Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44: 1-14.
50. 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.
51. Melchitzky DS, Lewis DA. 2003. Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons. Cereb Cortex 13: 452-460.
52. Meredith GE, Arbuthnott GW, editors. 1993. Morphological investigation of single neurons in vitro. IBRO Handbook Series. Methods in neuroscience, vol 16. New York: John Wiley & Sons.
53. Millenbruck JA, Wallinga MH. 1946. A newly developed anaesthetic for horses. J Am Vet Med Assoc 108: 148-151.
54. Miller MW. 1987. The origin of corticospinal projection neurons in rat. Exp Brain Res 67: 339-351.
55. Molnar Z, Cheung AFP. 2006. Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55: 105-115.
56. Neafsey EJ, Terreberry RR, Hurley KM, Ruit KG, Frysztak RJ. 1993. Anterior cingulate cortex in rodents: connections, visceral control functions, and implications for emotion. In Vogt BA, Gabriel M, editors. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook. Boston: Birkhauser. p 206-223.
57. Nudo RJ, Masterton RB. 1990. Descending pathways to the spinal cord, III: Sites of origin of the corticospinal tract. J Comp Neurol 296: 559-583.
58. Owens NC, Verberne AJ. 2001. Regional haemodynamic responses to activation of the medial prefrontal cortex depressor region. Brain Res 919: 221-231.
59. Ongur D, Price JL. 2000. The organisation of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10: 206-219.
60. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego, CA: Academic Press.
61. Paxinos G, Kus L, Ashwell KWS, Watson C. 1999. Chemoarchitectonic atlas of the rat forebrain. London: Academic Press.
62. Peters A, Palay SL, Webster H de F. 1991. The fine structure of the nervous system, neurons and their supporting cells. 3rd ed. Oxford: Oxford University Press.
63. Ragozzino ME, Adams S, Kesner RP, 1998. Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav Neurosci 112: 293-303.
64. Ragozzino ME, Wilcox C, Raso M, Kesner RP. 1999a. Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113: 32-41.
65. Ragozzino ME, Detrick S, Kesner RP. 1999b. Involvement of the prelimbic/infralimbic areas of the rodent prefrontal cortex in behavioural flexibility for place and response learning. J Neurosci 19: 4585-4594.
66. Saper CB, Swanson LW, Cowan WM. 1976. Direct hypothalamoautonomic connections. Brain Res 117: 305-312.
67. 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.
68. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. Topographical organisation of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 229: 242-256.
69. Sesack S, Medvitz N, Miner L, Ekema G. 2001. Pyramidal neuron intrinsic collaterals in the rat prefrontal cortex: synaptic targets and selective input to parvalbumin-containing interneurons. Soc Neurosci Abstr 27: 1930.
70. Swanson LW. 1998. Brain maps: structure of the rat brain. 2nd ed. Amsterdam: Elsevier.
71. Tanaka YH, Tanaka YR, Fujiyama F, Furuta T, Yanagawa Y, Kaneko T. 2011. Local connections of layer 5 GABAergic interneurons to corticospinal neurons. Front Neural Circuits 5: 12.
72. Uylings HBM, van Eden GG, de Bruin JPC, Feenstra MGP, Pennartz CMA, eds. 2000. Cognition, emotion and autonomic responses: the integrative role of the prefrontal cortex and limbic structures. Amsterdam: Elsevier.
73. Verberne AJM, Owens NC. 1998. Cortical modulation of the cardiovascular system. Prog Neurobiol 54: 149-168.
74. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51: 32-58.
75. Vogt BA, ed. 2009. Cingulate neurobiology and disease. Oxford: Oxford University Press.
76. Westerhaus MJ, Loewy AD. 2001. Central representation of the sympathetic nervous system in the cerebral cortex. Brain Res 903: 117-127.
77. Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, Krimer LS. 2005. Localization of calcium-binding proteins in physiologically and morphologicallycharacterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15: 1178-1186.