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Connections of the hippocampal formation, mamillary bodies, anterior thalamus and cingulate cortex

A retrograde study using horseradish peroxidase in the cat

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Summary

The afferent projections to, and the interconnections between, four structures of the socalled limbic system were investigated in the cat. The retrograde horseradish peroxidase (HRP) technique was used to trace the origins of fibers projecting to each of these four loci. Particular emphasis was laid on tracing cortical afferents of these regions. Four injections were performed in the dorsal and two in the ventral subicular regions; six were centered within the mamillary nuclei, four within the anterior thalamic nuclei, and three within the cingulate gyrus. For each region, a number of projections were found which had apparently not been described before, at least not for the cat:

For injections into the subicular regions, a hitherto unknown number of cortical afferents was detected, including labeled cells in the prefrontal and premotor fields and from large areas within the posterior parietal, temporal and occipital cortex (i.e., sensory and sensory integration cortex); numerous neurons were labeled in the anterior nuclear group of the thalamus. Injections of HRP into the mamillary nuclei revealed, aside from a strong projection from the subicular regions, frontocortical and cingulate projections to the mamillary nuclei; the mamillary nuclei also received subcortical projections from the septum, the diagonal band of Broca and from the periaqueductal gray. Following injections into the anterior thalamic nuclei, labeled cells were found in the prefrontal cortex, and to a lesser extent in lateral parts of the cortical hemisphere; subcortically, the mamillary nuclei received connections from hypothalamic areas, the periaqueductal gray, the diagonal band of Broca and the claustrum. Cingulate injections labeled cells in temporal and parietal cortical areas, in the subicular region, and also in the periaqueductal gray.

Our findings reveal that each of the four injected areas receives a large number of afferents from divergent regions of the brain; of these, a considerable number is shared by each of the four injection loci. Furthermore, the present results reveal that the subiculum, the mamillary bodies, and the anterior thalamus are more strongly interconnected than previously assumed.

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References

  • Adey WR (1951) An experimental study of the hippocampal connexions of the cingulate cortex in the rabbit. Brain 74: 233–248

    Google Scholar 

  • Adey WR, Meyer M (1952) An experimental study of hippocampal afferent pathways from prefrontal and cingulate areas in the monkey. J Anat 86: 58–75

    Google Scholar 

  • Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189: 573–591

    Google Scholar 

  • Baleydier C, Mauguière F (1980) The duality of the cingulate gyrus in monkey. Neuroanatomcial study and functional hypothesis. Brain 103: 525–554

    Google Scholar 

  • Barbizet J (1963) Defect of memorizing of hippocampal-mamillary origin: a review. J Neurol Neurosurg Psychiat 26: 127–135

    Google Scholar 

  • Beck E, Meyer A, Le Beau J (1951) Efferent connexions of the human prefrontal region with reference to frontohypothalamic pathways. J Neurol Neurosurg Psychiat 14: 295–302

    Google Scholar 

  • Berger TW, Swanson GW, Mimer TA, Lynch GS, Thompson RF (1980) Reciprocal anatomical connections between hippocampus and subiculum in the rabbit: Evidence for subicular innervation of regio superior. Brain Res 183: 265–276

    Google Scholar 

  • Berman AL (1968) The brain stem of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. University of Wisconsin Press, Madison

    Google Scholar 

  • Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105: 417–537

    Google Scholar 

  • Briggs TL, Kaelber WW (1971) Efferent fiber connections of the dorsal and deep tegmental nuclei of Gudden. An experimental study in the cat. Brain Res 29: 17–29

    Google Scholar 

  • Chronister RB, Sikes RW, White LE Jr (1975) Postcommissural fornix: origin and distribution in the rodent. Neurosci Lett 1: 199–202

    Google Scholar 

  • Conrad LCA, Pfaff DW (1976a) Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographie study of the medial preoptic area. J Comp Neurol 169: 185–220

    Google Scholar 

  • Conrad LCA, Pfaff DW (1976b) Efferents from medial basal forebrain and hypothalamus in the rat. II. An autoradiographie study of the anterior hypothalamus. J Comp Neurol 169: 221–262

    Google Scholar 

  • Cowan WM, Guillery RW, Powell TPS (1964) The origin of the mamillary peduncle and other hypothalamic connexions from the midbrain. J Anat 98: 345–363

    Google Scholar 

  • Cruce JAF (1975) An autoradiographic study of the projections of the mammillothalamic tract in the rat. Brain Res 85: 211–219

    Google Scholar 

  • Delay J, Brion S (1969) Le syndrome de Korsakoff. Masson, Paris

    Google Scholar 

  • DeVito JL (1980) Subcortical projections to the hippocampal formation in squirrel monkey (Saimiri sciureus). Brain Res Bull 5: 285–289

    Google Scholar 

  • Domesick VB (1969) Projections from the cingulate cortex in the rat. Brain Res 12: 296–320

    Google Scholar 

  • Drachman DA, Arbit J (1966) Memory and the hippocampal complex. Arch Neurol 15: 52–61

    Google Scholar 

  • Eccles JC (1978) An instruction-selection hypothesis of cerebral learning. In: Buser PA, Rougeul-Buser A (eds) Cerebral correlates of conscious experience. Elsevier/North-Holland, Amsterdam, pp 155–175

    Google Scholar 

  • Edinger HM, Kraemer SZ, Weiner S, Krayniak PF, Siegel A (1979) The subicular cortex of the cat: An anatomical and electrophysiological study. Exp Neurol 63: 504–526

    Google Scholar 

  • Fox CA (1941) The mammillary peduncle and ventral tegmental nucleus in the cat. J Comp Neurol 75: 411–425

    Google Scholar 

  • Hajdu F, Hassler R (1973) Fiber projections of the non-specific midline nuclei to the anterior dorsal nucleus of the thalamus in the cat. Exp Brain Res 17: 216–220

    Google Scholar 

  • Hamilton BL (1973) Projections of the nuclei of the periaqueductal gray matter in the cat. J Comp Neurol 152: 45–58

    Google Scholar 

  • Herkenham M (1978) The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol 177: 589–610

    Google Scholar 

  • Herkenham M, Nauta WJH (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19–48

    Google Scholar 

  • Hjorth-Simonsen A (1976) Laminar distribution and topical organization of intrinsic connections in the hippocampal region. Exp Brain Res [Suppl] 1: 171–176

    Google Scholar 

  • Jacobson S, Butters N, Tovsky NJ (1978) Afferent and efferent subcortical projections of behaviorally defined sectors of the prefrontal granular cortex. Brain Res 159: 279–296

    Google Scholar 

  • Jasper HH, Ajmone-Marsan CA (1954) A stereotaxic atlas of the diencephalon of the cat. Natl Res Counc Can, Ottawa

  • Jürgens U, Müller-Preuss P (1977) Convergent projections of different limbic vocalization areas in the squirrel monkey. Exp Brain Res 29: 75–83

    Google Scholar 

  • Kaitz SS, Robertson RT (1981) Thalamic connections with limbic cortex. II. Corticothalamic projections. J Comp Neurol 195: 527–545

    Google Scholar 

  • Kasdon DL, Jacobson S (1978) The thalamic afferents to the inferior parietal lobule of the rhesus monkey. J Comp Neurol 177: 685–706

    Google Scholar 

  • Keefer DA (1978) Horseradish peroxidase as a retrogradelytransported, detailed dendritic marker. Brain Res 140: 15–32

    Google Scholar 

  • Kievit J, Kuypers HGJM (1977) Organization of the thalamocortical connexions to the frontal lobe in the rhesus monkey. Exp Brain Res 29: 299–322

    Google Scholar 

  • Kuypers HGJM, Bentivoglio M, Catsman-Berrevoets CE, Bharos AT (1980) Double retrograde neuronal labeling through divergent axon collaterals, using two fluorescent tracers with the same excitation wavelength which label different features of the cell. Exp Brain Res 40: 383–392

    Google Scholar 

  • Laplane D, Degos JD, Baulac M, Gray F (1981) Bilateral infarction of the anterior cingulate gyri and the fornices. J Neurol Sci 51: 289–300

    Google Scholar 

  • Leichnetz GR, Astruc J (1975a) Preliminary evidence for a direct projection of the prefrontal cortex to the hippocampus in the squirrel monkey. Brain Behav Evol 11: 355–364

    Google Scholar 

  • Leichnetz GR, Astruc J (1975b) Efferent connections of the orbitofrontal cortex in the marmoset (Saguinus oedipus). Brain Res 84: 169–180

    Google Scholar 

  • Leichnetz GR, Astruc J (1976a) The efferent projections of the medial prefrontal cortex in the squirrel monkey (Saimiri sciureus). Brain Res 109: 455–472

    Google Scholar 

  • Leichnetz GR, Astruc J (1976b) The squirrel monkey entorhinal cortex: architecture and medial frontal afferents. Brain Res Bull 1: 351–358

    Google Scholar 

  • MacLean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroenceph Clin Neurophysiol 4: 407–418

    Google Scholar 

  • Mair WGP, Warrington EK, Weiskrantz L (1979) Memory disorder in Korsakoff's psychosis. A neuropathological and neuropsychological investigation of two cases. Brain 102: 749–783

    Google Scholar 

  • Markowitsch HJ (1982) The thalamic mediodorsal nucleus and memory: A critical evaluation of studies in animals and man. Neurosci Biobehav Rev (in press)

  • Markowitsch HJ, Irle E (1981) Widespread cortical projections of the ventral tegmental area and of other brain stem structures in the cat. Exp Brain Res 41: 233–246

    Google Scholar 

  • Markowitsch HJ, Pritzel M (1977) A stereotaxic atlas of the prefrontal cortex of the cat. Acta Neurobiol Exp 37: 63–81

    Google Scholar 

  • Markowitsch HJ, Pritzel M, Divac I (1978) The prefrontal cortex of the cat: Anatomical subdivisions based on retrograde labeling of cells in the mediodorsal thalamic nucleus. Exp Brain Res 32: 335–344

    Google Scholar 

  • Meibach RC, Siegel A (1977a) Efferent connections of the hippocampal formation in the rat. Brain Res 124: 197–224

    Google Scholar 

  • Meibach RC, Siegel A (1977b) Subicular projections to the posterior cingulate cortex in rats. Exp Neurol 57: 264–274

    Google Scholar 

  • Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26: 106–117

    CAS  PubMed  Google Scholar 

  • Mesulam M-M, Rosene DL (1979) Sensitivity in horseradish peroxidase neurohistochemistry: A comparative and quantitative study of nine methods. J Histochem Cytochem 27: 763–773

    Google Scholar 

  • Meyer M (1949) A study of efferent connexions of the frontal lobe in the human brain after leucotomy. Brain 72: 265–296

    Google Scholar 

  • Mizuno N, Clemente CD, Sauerland EK (1969) Fiber projections from rostral basal forebrain structures in the cat. Exp Neurol 25: 220–237

    Google Scholar 

  • Mosko S, Lynch G, Cotman CW (1973) The distribution of septal projections to the hippocampus of the rat. J Comp Neurol 152: 163–174

    Google Scholar 

  • Nauta WJH, Haymaker W (1969) Hypothalamic nuclei and fiber connections. In: Haymaker W, Anderson E, Nauta WJH (eds) The hypothalamus. Thomas, Springfield, IL, pp 136–209

    Google Scholar 

  • Niimi K, Niimi M, Okada Y (1978) Thalamic afferents to the limbic cortex in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. Brain Res 145: 225–238

    Google Scholar 

  • Niki H, Watanabe M (1976) Cingulate unit activity and delayed response. Brain Res 110: 381–386

    Google Scholar 

  • Pandya DN, Van Hoesen GW, Mesulam M-M (1981) Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res 42: 319–330

    Google Scholar 

  • Papez JW (1937) A proposed mechanism of emotion. Arch Neurol Psychiatr 38: 725–743

    Google Scholar 

  • Powell ER (1966) Septal efferents in the cat. Exp Neurol 14: 328–337

    Google Scholar 

  • Powell ER (1973) Limbic projections to the thalamus. Exp Brain Res 17: 394–401

    Google Scholar 

  • Powell ER, Akagi K, Hatten JB (1974) Subcortical projections of the cingulate gyrus in the cat. J Hirnforsch 15: 269–278

    Google Scholar 

  • Raisman G, Cowan WM, Powell TPS (1965) The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88: 963–996

    Google Scholar 

  • Raisman G, Cowan WM, Powell TPS (1966) An experimental analysis of the efferent projection of the hippocampus. Brain 89: 83–108

    Google Scholar 

  • Reinoso-Suárez F (1961) Topographischer Hirnatlas der Katze für experimental-physiologische Untersuchungen. Merck, Darmstadt

    Google Scholar 

  • Robertson RT, Kaitz SS (1981) Thalamic connections with limbic cortex. I. Thalamocortical projections. J Comp Neurol 195: 501–525

    Google Scholar 

  • Rose JE, Woolsey CN (1948) Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat. J Comp Neurol 89: 279–347

    Google Scholar 

  • Rosene DL, Van Hoesen GW (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198: 315–317

    Google Scholar 

  • Saper CB, Swanson LW, Cowan WM (1976) The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J Comp Neurol 169: 409–442

    Google Scholar 

  • Segal M (1977) Afferents to the entorhinal cortex of the rat studied by the method of retrograde transport of horseradish peroxidase. Exp Neurol 57: 750–765

    Google Scholar 

  • Siegel A, Tassoni JP (1971a) Differential efferent projections from the ventral and dorsal hippocampus of the cat. Brain Behav Evol 4: 185–200

    Google Scholar 

  • Siegel A, Tassoni JP (1971b) Differential efferent projections of the lateral and medial septal nuclei to the hippocampus in the cat. Brain Behav Evol 4: 201–219

    Google Scholar 

  • Snider RS, Niemer WT (1961) A stereotaxic atlas of the cat brain. Univ. of Chicago Press, Chicago

    Google Scholar 

  • Spiro T, Massopust LC, Young PA (1980) Efferent projections of the lateral dorsal nucleus in the rat. Exp Neurol 68: 171–184

    Google Scholar 

  • Stephan H (1975) Allocortex. Handbuch der mikroskopischen Anatomie des Menschen, vol IV/9. Springer, Berlin

    Google Scholar 

  • Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169: 347–370

    Google Scholar 

  • Swanson LW, Cowan WM (1975a) Hippocampo-hypothalamic connections: origin in subicular cortex, not Ammon's horn. Science 189: 303–304

    Google Scholar 

  • Swanson LW, Cowan WM (1975b) The efferent connections of the suprachiasmatic nucleus of the hypothalamus. J Comp Neurol 160: 1–12

    Google Scholar 

  • Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172: 49–84

    Google Scholar 

  • Sweet WH, Talland GA, Ervin FR (1959) Loss of recent memory following section of the fornix. Transact Am Neurol Ass 84: 76–82

    Google Scholar 

  • Tusa RJ, Rosenquist AC, Palmer LA (1979) Retinotopic organization of areas 18 and 19 in the cat. J Comp Neurol 185: 657–678

    Google Scholar 

  • Van Hoesen GW, Pandya DN (1975) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res 95: 39–59

    Google Scholar 

  • Van Hoesen GW, Rosene DL, Mesulam M-M (1979) Subicular input from temporal cortex in the rhesus monkey. Science 205: 608–610

    Google Scholar 

  • Vaz Ferraira A (1951) The cortical areas of the albino rat studied by silver impregnation. J Comp Neurol 95: 177–244

    Google Scholar 

  • Victor M, Adams RD, Coffins GH (1971) The Wernicke-Korsakoff syndrome. Blackwell, Oxford

    Google Scholar 

  • Victor M, Angevine J, Mancall E, Fisher CM (1961) Memory loss with lesions of hippocampal formation. Arch Neurol 5: 244–263

    Google Scholar 

  • Vogt BA, Rosene DL, Pandya DN (1979) Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the rhesus monkey. Science 204: 205–207

    Google Scholar 

  • Ward AA Jr, McCulloch WS (1947) The projection of the frontal lobe on the hypothalamus. J Neurophysiol 10: 309–314

    Google Scholar 

  • White LE, Jr (1959) Ipsilateral afferents to the hippocampal formation in the albino rat. I. Cingulum projections. J Comp Neurol 113: 1–41

    Google Scholar 

  • Wolf G, Sutin J (1966) Fiber degeneration after lateral hypothalamic lesions in the rat. J Comp Neurol 127: 137–156

    Google Scholar 

  • Wyss JM, Swanson LW, Cowan WM (1979) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4: 463–476

    Google Scholar 

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The mamillary bodies are spelled herein according to the suggestion given in the 4th edition of Nomina anatomica

Supported by grant Ma 795 of the Deutsche Forschungsgemeinschaft

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Irle, E., Markowitsch, H.J. Connections of the hippocampal formation, mamillary bodies, anterior thalamus and cingulate cortex. Exp Brain Res 47, 79–94 (1982). https://doi.org/10.1007/BF00235889

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