Research Article| Volume 60, P181-186, July 2016

Download started.


Differential responsiveness of the right parahippocampal region to electrical stimulation in fixed human brains: Implications for historical surgical stimulation studies?


      • Fixed human brains display frequency-specific current response.
      • Right hippocampus displayed increased gamma power to any frequency.
      • Right parahippocampal region responded exclusively to 7-Hz spikes.
      • Right parahippocampal region shows 7-Hz and 40-Hz response indicators.


      If structure dictates function within the living human brain, then the persistence of specific responses to weak electric currents in fixed, deceased brains could reflect “hardwired” properties. Different key structures from the left and right hemispheres of brains that had been fixed for over 20 years with ethanol–formalin–acetic acid were stimulated with either 1-Hz, 7-Hz, 10-Hz, 20-Hz, or 30-Hz, sine-wave, square-wave, or pulsed currents while needle-recorded quantitative electroencephalographic responses were obtained. Differential responses occurred only within the right hippocampus and parahippocampal gyrus. The right hippocampus displayed frequency-independent increases in gamma power relative to the left hemispheric homologue. The parahippocampal region responded exclusively to 7-Hz pulsed currents with wideband (8–30 Hz) power. These profiles are consistent with dynamic connections associated with memory and consciousness and may partially explain the interactions resultant of pulse type and hemisphere for experiential elicitations during the golden age of surgical stimulations. The results also indicate that there may be an essential “hardwiring” within the human brain that is maintained for decades when it is fixed appropriately.


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Epilepsy & Behavior
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Kubie L.S.
        Some implications for psychoanalysis of modern concepts of the organization of the brain.
        Psychoanal Q. 1953; 22: 21-68
        • Williams D.
        The structure of emotions reflected in epileptic experiences.
        Brain. 1956; 79: 29-67
        • Mahl G.F.
        • Rothenberg A.
        • Delgado J.M.R.
        • Hamlin H.
        Psychological responses in the human to intracerebral electrical stimulation.
        Psychosom Med. 1964; 26: 337-368
        • Horowitz M.J.
        • Adams J.E.
        Hallucinations on brain stimulation: evidence for revision of the Penfield hypothesis.
        in: Keup W. Origins and mechanisms of hallucinations. Plenum, N.Y.1970: 12-20
        • Gloor P.
        • Olivier A.
        • Quesney L.F.
        • Andermann F.
        • Horowitz S.
        The role of the limbic system in experiential phenomena of temporal lobe epilepsy.
        Ann Neurol. 1982; 12: 129-144
        • Gloor P.
        Temporal lobe epilepsy: its possible contribution to the understanding of the functional significance of the amygdala and its interaction with neocortical–temporal mechanisms.
        in: Eleftherion B.E. Advances in behavioral biology: the neurobiology of the amygdala. Plenum Press, N.Y.1972: 423-457
        • Halgren E.
        • Walter R.D.
        • Cherlow D.G.
        • Crandal P.H.
        Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala.
        Brain. 1978; 101: 83-117
        • Bancaud J.
        • Brunet-Bourgin F.
        • Chauvel P.
        • Halgren E.
        Anatomical origin of déjà vu and vivid “memories” in human temporal lobe epilepsy.
        Brain. 1994; 117: 71-90
        • Stevens J.R.
        • Mark V.H.
        • Erwin F.
        • Pacheco P.
        • Suematsu K.
        Deep temporal stimulation in man.
        Arch Neurol. 1969; 21: 157-169
        • Weiser H.G.
        Depth recorded limbic seizures and psychopathology.
        Neurosci Biobehav Rev. 1983; 7: 427-440
        • Babb T.L.
        • Wilson C.L.
        • Isokawa-Akesson M.
        Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical temporal lobe seizures.
        Electroencephalogr Clin Neurophysiol. 1987; 66: 467-482
        • Isokawa-Akesson M.
        • Wilson C.L.
        • Babb T.L.
        Structurally stable burst and synchronized firing in human amygdaloid neurons: autocorrelation analyses in temporal lobe epilepsy.
        Epilepsy Res. 1987; 1: 17-34
        • Lieb J.P.
        • Hoque K.
        • Skomer C.E.
        • Song X.-W.
        Interhemispheric propagation of human mesial temporal lobe seizures: a coherence/phase analysis.
        Electroencephalogr Clin Neurophysiol. 1987; 67: 101-119
        • Persinger M.A.
        Brain mast cells in the albino rat: sources of variability.
        Behav Neural Biol. 1979; 25: 380-386
        • Bear D.M.
        Temporal lobe epilepsy — a syndrome of sensory–limbic hyperconnectionism.
        Cortex. 1979; 15: 357-384
        • Harrison P.T.C.
        An ethanol–acetic acid–formol saline fixative for routine use with special application to the fixation of non-perfused rat lung.
        Lab Anim. 1984; 18: 325-331
        • Fernandez F.R.
        • Malerba P.
        • Bressloff P.C.
        • White J.A.
        Entorhinal stellate cells show preferred spike phase-locking to theta inputs that is enhanced by correlations in synaptic activity.
        J Neurosci. 2013; 33: 6027-6040
        • Nunez P.L.
        Towards a physics of the neocortex.
        in: Nunez P.L. Neocortical dynamics and human EEG rhythms. Oxford University Press, Oxford1995: 68-132
        • Llinas R.
        • Ribary U.
        Coherent 40-Hz oscillation characterizes dream state in humans.
        Proc Natl Acad Sci. 1993; 90: 2078-2081
        • Llinas R.R.
        • Pare D.
        Of dreaming and wakefulness.
        Neuroscience. 1991; 44: 521-535
        • Tsang E.W.
        • Koren S.A.
        • Persinger M.A.
        Power increases within the gamma range over the frontal and occipital regions during acute exposures to cerebrally counterclockwise rotating magnetic fields with specific derivatives of change.
        Int J Neurosci. 2004; 114: 1183-1193
        • Buzsaki G.
        Theta oscillations in the hippocampus.
        Neuron. 2002; 33: 325-340
        • Holtz E.M.
        • Glennon M.
        • Prendergast K.
        • Sauseng P.
        Theta–gamma phase synchronization during memory matching in visual working memory.
        Neuroimage. 2010; 52: 326-335
        • Whitman J.C.
        • Ward L.M.
        • Woodward T.S.
        Patterns of cortical oscillations organize neural activity in whole-brain functional networks evident in the fMRI BOLD signal.
        Front Hum Neurosci. 2013; 7 ([Article 80])
        • Greenough W.T.
        Structural correlates of information storage in the mammalian brain: a review and hypothesis.
        Trends Neurosci. 1984; 7: 229-233
        • Rose G.M.
        • Diamond D.M.
        • Pang K.
        • Dundwiddie T.V.
        Primed burst potentiation: lasting synaptic plasticity invoked by physiologically patterned stimuli.
        in: Haas H.L. Buzsaki G. Synaptic plasticity in the hippocampus. Springer-Verlag, Berlin1988: 96-98
        • Whitlock J.R.
        • Heynen A.J.
        • Shuler M.G.
        • Bear M.F.
        Learning induces long-term potentiation in the hippocampus.
        Science. 2006; 313: 1093-1098
        • Bragin A.
        • Engel J.
        • Wilson C.L.
        • Fried I.
        • Buzaski G.
        High-frequency oscillation in human brain.
        Hippocampus. 1999; 9: 137-142
        • Bragin A.
        • Wilson C.L.
        • Staba R.J.
        • Reddick M.S.
        • Fried I.
        • Engel J.
        Interictal high-frequency oscillations (80 to 500 Hz) in the human epileptic brain: entorhinal cortex.
        Ann Neurol. 2002; 52: 407-415
        • Gloor P.
        The temporal lobe and limbic system.
        Oxford University Press, Oxford1997
        • Bear M.F.
        A synaptic basis for memory storage in the cerebral cortex.
        Proc Natl Acad Sci U S A. 1996; 93: 13453-13459
        • Goldberg E.
        • Roediger D.
        • Kucukboyaci N.E.
        • Carlson C.
        • Devinsky O.
        • Kuzniecky R.
        • et al.
        Hemispheric asymmetries of cortical volume in the human brain.
        Cortex. 2013; 49: 200-210
        • Good C.D.
        • Johnsrude I.
        • Ashburner J.
        • Henson R.N.A.
        • Friston D.J.
        • Frackowiak S.J.
        Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult brains.
        Neuroimage. 2001; 14: 685-700
        • Bear D.M.
        Hemispheric asymmetries in emotional function: a reflection of lateral specialization in cortical–limbic connections.
        in: Doane B.K. Livingston K.E. The limbic system: functional organization and clinical disorders. Raven, N.Y.1986: 29-42
        • Giocomo L.M.
        • Roudi Y.
        The neural coding of space in the parahippocampal cortices.
        Front Neural Circ. 2012; 6 ([Article 53])
      1. Rouleau N, Lehman, B, Persinger MA. Focal attenuation of specific electroencephalographic power over the right parahippocampal region during transcerebral copper screening in living subjects and hemispheric asymmetric voltages in fixed brain tissue. Brain Res. [in review] 2016.

        • Mulligan B.P.
        • Hunter M.D.
        • Persinger M.A.
        Effects of geomagnetic activity and atmospheric power variations on quantitative measures of brain activity: replication of Azerbijani studies.
        Adv Space Res. 2010; 45: 940-948
        • Mulligan B.P.
        • Persinger M.A.
        Experimental simulation of the effects of sudden increases in geomagnetic activity upon quantitative measures of human brain activity: validation of correlational studies.
        Neurosci Lett. 2012; 516: 54-56