Experimental Brain Research

, Volume 82, Issue 2, pp 279–292 | Cite as

Functional connections in the human temporal lobe

I. Analysis of limbic system pathways using neuronal responses evoked by electrical stimulation
  • C. L. Wilson
  • M. Isokawa
  • T. L. Babb
  • P. H. Crandall
Article

Summary

Connections in the human mesial temporal lobe were investigated using brief, single pulses of electrical stimulation to evoke field potential responses in limbic structures of 74 epileptic patients. Eight specific areas within these structures were stereotactically targeted for study, including amygdala, entorhinal cortex, presubiculum, the anterior, middle and posterior levels of hippocampus and the middle and posterior levels of parahippocampal gyrus. These sites were studied systematically in order to quantitatively assess the response characteristics and reliability of responses evoked during stimulation of pathways connecting the areas. Specific measures included response probability, amplitude, latency and conduction velocities. The results are assumed to be representative of typical human limbic pathways since all recordings were made interictally and response probabilities across sites were not found to differ significantly between non-epileptogenic vs. identified epileptogenic regions. Field potentials ranging in amplitude from less than 0.1 to greater than 6.0 mV were evoked ipsilaterally, with mean onset latencies and conduction velocities ranging from 4.4 ms and 3.64 m/s in the perforant pathway connecting entorhinal cortex to anterior hippocampus to 24.8 ms and 0.88 m/s in the pathway connecting the amygdala and middle hippocampus. Stimulation of presubiculum and entorhinal cortex were most effective in evoking widespread responses in adjacent limbic recording sites, whereas posterior parahippocampal gyrus appeared functionally separated from other limbic sites since its probability of influencing ipsilateral sites was significantly lower than any other area. It was particularly noteworthy that stimulation did not evoke responses in any sites in contralateral hippocampal formation; even though a large number of sites were tested with bilateral implantation of homotopic electrodes. The absence of evidence for a functional contralateral limbic projection in the human brain stands in marked contrast to the anatomical and physiological evidence in lower animals for strong contralateral connections between subfields of the hippocampus via the hippocampal commissure. In addition, it correlates well with anatomical evidence for reduced hippocampal commissural connections in lower primates.

Key words

Human temporal lobe Hippocampus Amygdala Subiculum Electrical stimulation Evoked potentials 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison T, Wood CC, McCarthy G, Hume G, Goff WR (1982) Short-latency somatosensory evoked potentials in man, monkey, cat, and rat: comparative latency analysis. In: Courjon J, Mauguiere F, Revol M (eds) Clinical applications of evoked potentials in neurology. Raven Press, New York, pp 303–311Google Scholar
  2. Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591Google Scholar
  3. Amaral DG, Insausti R (1990) The hippocampal formation. In: Paxinos G (eds) The human nervous system. Academic Press, New York, pp 711–755Google Scholar
  4. Amaral DG, Insausti R, Cowan WM (1984) The commissural connections of the monkey hippocampal formation. J Comp Neurol 224:307–336Google Scholar
  5. Andersen P (1959) Interhippocampal impulses. I. Origin, course and distribution in cat, rabbit and rat. Acta Physiol Scand 47:63–90Google Scholar
  6. Andersen P (1960) Interhippocampal impulses. IV. A correlation of some functional and structural properties of the interhippocampal fibers in cat, rabbit and rat. Acta Physiol Scand 48:329–351Google Scholar
  7. Andersen P, Bland BH, Dudar JD (1973) Organization of the hippocampal outputs. Exp Brain Res 17:152–168Google Scholar
  8. Andersen P, Bruland H, Kaada BR (1961) Activation of the dentata area by septal stimulation. Acta Physiol Scand 51:17–28Google Scholar
  9. Andersen P, Holmqvist B, Voorhoeve PE (1966) Excitatory synapses on hippocampal apical dendrites activated by entorhinal stimulation. Acta Physiol Scand 66:461–472Google Scholar
  10. Andersen P, Silfvenius H, Sundberg SH, Wigström H (1978) Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res 144:11–18.Google Scholar
  11. Andy OJ, Stephan H (1968) The septum in the human brain. J Comp Neurol 133:383–410Google Scholar
  12. Ariens-Kappers CU, Huber GC, Crosby EC (1960) The comparative anatomy of the nervous system of vertebrates, including man, Vol III. Hafner, New York, pp 1401–1437Google Scholar
  13. Babb TL, Crandall PH (1976) Epileptogenesis of human limbic neurons in psychomotor epileptics. Electroencephalogr Clin Neurophysiol 40:225–243Google Scholar
  14. Babb TL, Kupfer W (1984a) Phagocytic and metabolic reactions to chronically implanted metal brain electrodes. Exp Neurol 86:171–182Google Scholar
  15. Babb TL, Kupfer W (1984b) Phagocytic and metabolic reactions to intracerebral electrical stimulation of rat brain. Exp Neurol 86:183–197Google Scholar
  16. Babb TL, Carr E, Crandall PH (1973) Analysis of extracellular firing patterns of deep temporal lobe structures in man. Electroencephalogr Clin Neurophysiol 34:247–257Google Scholar
  17. Babb TL, Mariani Seidner KA, Mutafyan G, Halgren E, Wilson CL, Crandall PH (1980) A circuit for safe diagnostic electrical stimulation of the human brain. Neurol Res 2:181–197Google Scholar
  18. Babb TL, Pretorius JK, Kupfer WR, Brown WJ (1988) Distribution of glutamate-decarboxylase-immunoreactive neurons and synapses in the rat and monkey hippocampus: light and electron microscopy. J Comp Neurol 278:121–138Google Scholar
  19. Bartesaghi R, Gessi T (1986) Hippocampal output to the subicular cortex: an electrophysiological study. Exp Neurol 92:114–133Google Scholar
  20. Bartesaghi R, Gessi T, Sperti L (1983) Interlamellar transfer of impulses in the hippocampal formation. Exp Neurol 82:550–567Google Scholar
  21. Bernier GP, Saint-Hilaire JM, Girard N, Bouvier G, Mercier M (1987) Commentary: intracranial electrical stimulation. In: Engel J Jr (eds) Surgical treatment of the epilepsies. Raven Press, New York, pp 323–334Google Scholar
  22. Blackstad TW (1956) Commissural connections of the hippocampal region in the rat with special reference to their mode of termination. J Comp Neurol 105:417–538Google Scholar
  23. Brazier MAB (1964) Evoked responses from the depths of the human brain. Ann NY Acad Sci 112:33–5Google Scholar
  24. Brazier MAB (1972) Spread of seizure discharges in epilepsy: anatomical and electrophysiological considerations. Exp Neurol 36:263–272Google Scholar
  25. Brazier MAB (1973) Electrical seizure discharges within the human brain: the problem of spread. In: Brazier MAB (eds) Epilepsy — its phenomena in man. Academic Press, New York, pp 153–170Google Scholar
  26. Brothers LA, Finch DM (1985) Physiological evidence for an excitatory pathway from entorhinal cortex to amygdala in the rat. Brain Res 359:10–20Google Scholar
  27. Buser P, Bancaud J (1983) Unilateral connections between amygdala and hippocampus in man. Electroencephalogr Clin Neurophysiol 55:1–12Google Scholar
  28. Buser P, Bancaud J, Talairach J (1973) Depth recordings in man in temporal lobe epilepsy. In: Brazier MAB (eds) Epilepsy — its phenomena in man. Academic Press, New York, pp 67–97Google Scholar
  29. Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol (NY) 22:131–153Google Scholar
  30. Buzsáki G, Czéh G (1981) Commissural and perforant path interactions in the rat hippocampus. Exp Brain Res 43:429–438Google Scholar
  31. Buzsáki G, Eidelberg E (1981) Commissural projections to the dentate gyrus of the rat: evidence for feed-forward inhibition. Brain Res 230:346–350Google Scholar
  32. Buzsáki G, Leung LWS, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 6:139–171Google Scholar
  33. Cherlow DG, Dymond AM, Crandall PH, Walter RD, Serafetinides EA (1977) Evoked response and after-discharge thresholds to electrical stimulation in temporal lobe epileptics. Arch Neurol 34:527–531Google Scholar
  34. Crandall PH (1987) Cortical resections In: Engel J Jr (eds) Surgical treatment of the epilepsies. Raven Press, New York, pp 377–404Google Scholar
  35. Crosby EC (1982) Telencephalon of primates. In: Crosby EC, Schnitzlein HN (eds) Comparative correlative neuroanatomy of the vertebrate telencephalon. MacMillan, New York, pp 620–693Google Scholar
  36. Deadwyler SA, West JR, Cotman CW, Lynch G (1975) Physiological studies of the reciprocal connections between the hippocampus and entorhinal cortex. Exp Neurol 49:35–57Google Scholar
  37. Demeter S, Rosene DL, Van Hoesen GW (1985) Interhemispheric pathways of the hippocampal formation, presubiculum, and entorhinal and posterior parahippocampal cortices in the rhesus monkey: the structure and organization of the hippocampal commissures. J Comp Neurol 233:30–47Google Scholar
  38. Duvernoy HM (1988) The human hippocampus. JF Bergmann Verlag, MünchenGoogle Scholar
  39. Elul R (1964a) Regional differences in the hippocampus of the cat. I. Specific discharge patterns of the dorsal and ventral hippocampus and their role in generalized seizures. Electroencephalogr Clin Neurophysiol 16:470–488Google Scholar
  40. Elul R (1964b) Regional differences in the hippocampus of the cat. II. Projections of the dorsal and ventral hippocampus. Electroencephalogr Clin Neurophysiol 16:489–502Google Scholar
  41. Engel J Jr, Crandall PH (1986) Intensive neurodiagnostic monitoring with intracranial electrodes. In: Gumnit RJ (eds) Intensive neurodiagnostic monitoring, Vol 46. Raven Press, New York, pp 85–106Google Scholar
  42. Engel J, Crandall R, Rausch R (1983) The partial epilepsies. In: Rosenberg GW, Grossman RG, Schachet S, Heinz ER, Willis WD (eds) The clinical neurosciences, Vol II. Churchill Livingstone, New York, pp 1349–1380Google Scholar
  43. Engel J Jr, Ojemann GA, Lüders HO, Williamson PD (eds) (1987) fundamental mechanisms of human brain function: surgical treatment of epilepsy as an investigative resource. Raven Press, New YorkGoogle Scholar
  44. Engel J, Rausch R, Lieb JP, Kuhl DE, Crandall PH (1981) Correlation of criteria used for localizing epileptic foci in patients considered for surgical therapy of epilepsy. Ann Neurol 9:915–224Google Scholar
  45. Finch DM, Wong EE, Derian EL, Babb TL (1986 a) Neurophysiology of limbic system pathways in the rat: projections from the subicular complex and hippocampus to the entorhinal cortex. Brain Res 397:205–213Google Scholar
  46. Finch DM, Wong EE, Derian EL, Chen XH, Nowlin-Finch NL, Brothers LA (1986b) Neurophysiology of limbic system pathways in the rat: projections from the amygdala to the entorhinal cortex. Brain Res 370:273–284Google Scholar
  47. Fuller JH, Schlag JD (1976) Determination of antidromic excitation by the collision test: problems of interpretation. Brain Res 112:283–298Google Scholar
  48. Gessi T, Sperti L, Volta F (1966) Local response of the hippocampal cortex to direct stimulation in the guinea pig. Arch Sci Biol (Bologne) 50:20–40Google Scholar
  49. Gloor P (1955) Electrophysiological studies on the connection of the amygdaloid nucleus in the cat. Electroencephalogr Clin Neurophysiol 7:243–264Google Scholar
  50. Gloor P, Verra CL, Sperti L (1963) Configuration and laminar analysis of the “resting” potential gradient of the main transient response to perforant path, fimbrial and mossy fibre volley and of “spontaneous” activity. Electroencephalogr Clin Neurophysiol 15:353–378Google Scholar
  51. Goddard G, McIntyre D, Leech C (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295–330CrossRefPubMedGoogle Scholar
  52. Halgren E, Babb TL, Crandall PH (1978) Human hippocampal formation EEG desynchronizes during attentiveness and movement. Electroencephalogr Clin Neurophysiol 44:778–781Google Scholar
  53. Hofman MA (1982) Encephalization in mammals in relation to the size of the cerebral cortex. Brain Behav Evol 20:84–96Google Scholar
  54. Kandel E, Spencer WA (1961) Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol 24:243–259Google Scholar
  55. Köhler C, Shipley MT, Srebro B, Harkmark W (1978) Some retrohippocampal afferents to the entorhinal cortex cells of origin as studied by the HRP method in the rat and mouse. Neurosci Lett 10:115–120Google Scholar
  56. Leung LS (1979) Potentials evoked by alvear tract in hippocampal CA1 region of rats. I. Topographical projection, component analysis, and correlation with unit activities. J Neurophysiol 42:1557–1570Google Scholar
  57. Lieb JP, Babb TL (1986) Interhemispheric propagation time of human hippocampal seizures. II. Relationship to pathology and cell density. Epilepsia 27:294–300Google Scholar
  58. Lieb JT, Engel J, Babb TL (1986) Interhemispheric propagation time of human hippocampal seizures. I. Relationship to surgical outcome. Epilepsia 27:286–293Google Scholar
  59. Lieb JP, Babb TL, Engel J, Darcey T (1987) Propagation pathways of interhemispheric seizure discharges compared in human and animal hippocampal epilepsy. In: Engel J Jr, Ojemann GA, Lüders HO, Williamson PD (eds) Fundamental mechanisms of human brain function: surgical treatment of epilepsy as an investigative resource. Raven Press, New York, pp 165–170Google Scholar
  60. Lomo T (1971) Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp Brain Res 12:18–45Google Scholar
  61. Pandya DN, Rosene DL (1985) Some observations on trajectories and topography of commissural fibers. In: Reeves AG (eds) Epilepsy and the corpus callosum. Plenum Press, New York, pp 21–40Google Scholar
  62. Parmeggiani PL, Azzaroni A, Lenzi P (1971) On the functional significance of the circuit of Papez. Brain Res 30:357–374Google Scholar
  63. Raisman G, Cowan WM, Powell TPS (1965) The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88:963–998Google Scholar
  64. Ribak CE, Seress L, Peterson GM, Seroogy KB, Fallon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J Neurosci 12:3492–3498Google Scholar
  65. Rosene DL, Van Hoesen GW (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198:315–317Google Scholar
  66. Rosene DL, Van Hoesen GW (1987) The hippocampal formation of the primate brain. In: Jones EG, Peters A (eds) The cerebral cortex. Plenum, New York, pp 345–456Google Scholar
  67. Rutecki PA, Grossman RG, Armstrong D, Irish-Loewen S (1989) Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J Neurosurg 70:667–675Google Scholar
  68. Spencer SS (1988) Cortical and intercortical seizure spread. In: Meldrum BS, Ferrendelli J, Wieser HG (eds) The anatomy of epileptogenesis. John Libbey-Eurotext, LondonGoogle Scholar
  69. Stephan H, Andy OJ (1964) Quantitative comparisons of brain structures from insectivores to primates. Am Zool 4:59–74Google Scholar
  70. Steward O (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167:285–314Google Scholar
  71. Steward O (1981) Horseradish peroxidase and fluorescent substances and their combination with other techniques. In: Edwards SB, Hendrickson A (eds) The autoradiographic tracing of axonal connections in the central nervous system: neuroanatomy tract-tracing methods. Plenum, New York, pp 171–206Google Scholar
  72. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347–370Google Scholar
  73. Talairach J, David M, Tournoux P (1958) L'exploration chirurgicale stéréotaxique du lobe temporale dans l'épilepsie temporale: repérage anatomique stéréotaxique et technique chirurgicale. Masson et Cie, ParisGoogle Scholar
  74. Tielen AM, Lopes da Suva FH, Mollevanger WJ (1981) Differential conduction velocities in perforant path fibers in guinea pig. Exp Brain Res 42:231–33Google Scholar
  75. Van Groen T, Lopes da Silva FH (1985) Septotemporal distribution of entorhinal projections to the hippocampus in the cat: electrophysiological evidence. J Comp Neurol 238:1–9Google Scholar
  76. Van Groen T, Lopes da Silva FH (1986) Organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat. II. An electrophysiological study. J Comp Neurol 251:111–120Google Scholar
  77. Van Groen TV, Wyss JM (1988) Species differences in hippocampal commissural connections: studies in rat, guinea pig, rabbit, and cat. J Comp Neurol 267:322–334Google Scholar
  78. Van Hoesen GW, Pandya DN (1975a) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res 95:1–24Google Scholar
  79. Van Hoesen GW, Pandya DN (1975b) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res 95:39–59Google Scholar
  80. von Euler C, Green JD (1960) Excitation, inhibition and rhythmical activity in hippocampal pyramidal cells in rabbit. Acta Physiol Scand 48:110–125Google Scholar
  81. Wang ML, Wilson CL, Babb TL, Crandall PH (1981) Functional connections in the human limbic system. Neurosci Abstr 7:82Google Scholar
  82. West MJ, Schwerdtfeger WK (1985) An allometric study of hippocampal components: a comparative study of the brains of the European hedgehog (Erinaceus europaeus), the tree shrew (Tupaia glis), and the marmoset monkey (Callithrix jacchus). Brain Behav Evol 27:93–105Google Scholar
  83. Wieser HG (1983) Electroclinical features of the psychomotor seizure. G Fischer-Butterworths, Stuttgart LondonGoogle Scholar
  84. Wieser HG (1988) Human limbic seizures: EEG studies, origin and patterns of spread. In: Meldrum BS, Ferrendelli JA, Wieser HG (eds) Anatomy of epileptogenesis. John Libbey, London, pp 127–138Google Scholar
  85. Wieser HG, Bancaud J, Talairach J, Bonis A, Szikla G (1979) Comparative value of spontaneous and electrically induced seizures in establishing the lateralization of temporal lobe seizures. Epilepsia 20:47–59Google Scholar
  86. Wilson CL, Isokawa-Akesson M, Babb TL, Engel J Jr, Cahan LD, Crandall PH (1987) A comparative view of local and interhemispheric limbic pathways in humans: an evoked potential analysis. In: Engel J Jr, Ojemann GA, Lüders HO, Williamson PD (eds) Fundamental mechanisms of human brain function: opportunities for direct investigation in association with the surgical treatment of epilepsy. Raven Press, Stuttgart London, pp 27–38Google Scholar
  87. Wilson CL, Isokawa-Akesson M, Wang ML, Babb TL, Engel J Jr (1985) Lack of functional evidence for a human hippocampal commissure. Electroencephal Clin Neurophysiol 61:854Google Scholar
  88. Witter MP, Van Hoesen GW, Amaral DG (1989) Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci 9:216–228Google Scholar
  89. Wyss JM, Swanson LW, Cowan WM (1980) The organization of the fimbria, dorsal fornix and ventral hippocampal commissure in the rat. Anat Embryol 158:303–316Google Scholar
  90. Yamamoto C (1972) Activation of hippocampal neurons by mossy fibre stimulation in thin brain sections in vitro. Exp Brain Res 14:423–435Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • C. L. Wilson
    • 1
    • 2
  • M. Isokawa
    • 2
  • T. L. Babb
    • 1
    • 2
  • P. H. Crandall
    • 1
    • 2
    • 3
  1. 1.Department of NeurologyReed Neurological Research Center, University of CaliforniaLos AngelesUSA
  2. 2.Brain Research InstituteUniversity of CaliforniaLos AngelesUSA
  3. 3.Division of Neurological SurgeryCenter for the Health Sciences, University of CaliforniaLos AngelesUSA

Personalised recommendations