Findings from recordings of human temporal cortical single neuron activity during several measures of language, including object naming and word reading are reviewed and related to changes in activity in the same neurons during recent verbal memory and verbal associative learning measures, in studies conducted during awake neurosurgery for the treatment of epilepsy. The proportion of neurons changing activity with language tasks was similar in either hemisphere. Dominant hemisphere activity was characterized by relative inhibition, some of which occurred during overt speech, possibly to block perception of one’s own voice. However, the majority seems to represent a dynamic network becoming active with verbal memory encoding and especially verbal learning, but inhibited during performance of overlearned language tasks. Individual neurons are involved in different networks for different aspects of language, including naming or reading and naming in different languages. The majority of the changes in activity were tonic sustained shifts in firing. Patterned phasic activity for specific language items was very infrequently recorded. Human single neuron recordings provide a unique perspective on the biologic substrate for language, for these findings are in contrast to many of the findings from other techniques for investigating this.
References
[1]
Haglund, M.M.; Ojemann, G.A.; Hochman, D.W. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 1992, 358, 668–671.
[2]
Giussani, C.; Roux, F.E.; Ojemann, J.; Sganzerla, E.P.; Pirillo, D.; Papagno, C. Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic imaging and direct cortical stimulation studies. Neurosurgery 2010, 66, 113–120, doi:10.1227/01.NEU.0000360392.15450.C9.
[3]
Ojemann, G.A.; Corina, D.P.; Corrigna, N.; Schoenfield-McNeill, J.; Poliakov, A.; Zamora, L.; Zanos, S. Neuronal correlates of functional magnetic resonance imaging in human temporal cortex. Brain 2010, 133, 46–59, doi:10.1093/brain/awp227.
[4]
Ojemann, G.A. Awake operations with mapping in epilepsy. In Operative Neurosurgical Techniques, 3rd; Schmidek, H.H., Sweet, W.H., Eds.; W.B. Saunders Co.: Philadelphia, PA, USA, 1995; pp. 1317–1322.
[5]
Ojemann, G.; Ojemann, J.; Lettich, E.; Berger, M. Cortical language localization in left, dominant hemisphere: An electrical stimulation mapping investigation in 117 patients. J. Neurosurg. 1989, 71, 316–326, doi:10.3171/jns.1989.71.3.0316.
[6]
Fuster, J.M.; Jervey, J.P. Neuronal firing in the infertemporal cortex of the monkey in a visual memory task. J. Neurosci. 1982, 2, 361–375.
[7]
Ward, A.A., Jr.; Thomas, L.B. The electrical activity of single units in the cerebral cortex of man. Electroencephalogr. Clin. Neurophysiol. 1955, 7, 135–136, doi:10.1016/0013-4694(55)90067-5.
[8]
Ward, A.A., Jr.; Schmidt, R.P. Some Properties of Single Epileptic Neurons. Arch. Neurol. 1961, 5, 308–313, doi:10.1001/archneur.1961.00450150074010.
[9]
Calvin, W.H.; Ojemann, G.A.; Ward, A.A., Jr. Human cortical neurons in epileptogenic foci: Comparison of interictal firing patterns to those of “epileptic” neurons in animals. Electroencephalogr. Clin. Neurophysiol. 1973, 34, 337–351, doi:10.1016/0013-4694(73)90086-2.
[10]
Bechtereva, N.P.; Bundzen, P.V.; Matveev, Y.K.; Kaplunovsky, A.S. The functional reorganization of activity in neuronal populations of the human brain in short-term verbal memory (in Russian). Fiziol. Zh. SSSR Im. I M Sechenova 1971, 57, 1745–1761.
[11]
Halgren, E.; Babb, T.; Crandall, P.H. Activity of human hippocampal formation and amygdala neurons during memory testing. Electroencephalogr. Clin. Neurophysiol. 1978, 45, 585–601.
[12]
Ojemann, G.A.; Creutzfeldt, O.D.; Lettich, E.; Haglund, M.M. Neuronal activity in human lateral temporal cortex related to short-term verbal memory, naming and reading. Brain 1988, 111, 1383–1403, doi:10.1093/brain/111.6.1383.
[13]
Mukamel, R.; Fried, I. Human intracranial recording and cognitive neuroscience. Annu. Rev. Psychol. 2012, 63, 511–537, doi:10.1146/annurev-psych-120709-145401.
[14]
Creutzfeldt, O.; Ojemann, G.; Lettich, E. Neuronal activity in the human lateral temporal lobe: I. Responses to speech. Exp. Brain Res. 1989, 77, 451–475, doi:10.1007/BF00249600.
[15]
Creutzfeldt, O.; Ojemann, G.; Lettich, E. Neuronal activity in the human lateral temporal lobe: II. Responses to the subjects own voice. Exp. Brain Res. 1989, 77, 476–489, doi:10.1007/BF00249601.
[16]
Ojemann, J.; Ojemann, G.; Lettich, E. Neuronal activity related to faces and matching in human right nondominant temporal cortex. Brain 1992, 115, 1–13.
[17]
Haglund, M.M.; Ojemann, G.A.; Schwartz, T.W.; Lettich, E. Neuronal activity in human lateral temporal cortex during serial retrieval from short-term verbal memory. J. Neurosci. 1994, 14, 1507–1515.
[18]
Schwartz, T.; Ojemann, G.; Haglund, M.; Lettich, E. Cerebral lateralization of neuronal activity during naming, reading and line-matching. Brain Res. Cogn. Brain Res. 1996, 4, 263–273, doi:10.1016/S0926-6410(96)00062-6.
[19]
Ojemann, G.; Schoenfield-McNeill, J. Activity of neurons in human temporal cortex during identification and memory for names and words. J. Neurosci. 1999, 19, 5674–5682.
[20]
Weber, P.; Ojemann, G.A. Neuronal recordings in human lateral temporal lobe during verbal paired associates learning. NeuroReport 1995, 6, 685–689, doi:10.1097/00001756-199503000-00025.
[21]
Ojemann, G.A.; Schoenfield-McNeil, J. Neurons in human temporal cortex active with verbal associative learning. Brain Lang. 1998, 64, 317–327, doi:10.1006/brln.1998.1982.
[22]
Schwartz, T.H.; Haglund, M.M.; Lettich, E.; Ojemann, G.A. Asymmetry of neuronal activity during extracellular microelectrode recording from left and right human temporal lobe neocortex during rhyming and line matching. J. Cogn. Neurosci. 2000, 12, 803–812, doi:10.1162/089892900562615.
[23]
Ojemann, G.A. Organization of language cortex derived from investigations during neurosurgery. Semin. Neurosci. 1990, 2, 297–305.
[24]
Ojemann, G.A. Some brain mechanisms for reading. In Brain and Reading; von Euler, C., Lundberg, I., Lennerstrand, G., Eds.; MacMillan Press Ltd.: Hampshire, UK, 1989; pp. 47–59.
[25]
Bechtereva, N.P.; Abdullaev, Y.G.; Medvedev, S.V. Properties of neuronal activity in cortex and subcortical nuclei of the human brain during single-word processing. Electroencephalogr. Clin. Neurophysiol. 1992, 82, 296–301.
[26]
Lucas, T.H.; Schoenfield-McNeill, J.; Weber, P.B.; Ojemann, G.A. A direct measure of human lateral temporal lobe neurons responsive to face matching. Cogn. Brain Res. 2003, 18, 15–25, doi:10.1016/j.cogbrainres.2003.08.009.
Lucas, T.H., II; McKhann, G.M., II; Ojemann, G.A. Functional separation of languages in the bilingual brain: A comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients. J. Neurosurg. 2004, 101, 449–457.
[29]
Rizzolatti, G.; Camarda, R.; Fogass, L.; Gentilucci, M.; Lippino, G.; Matelli, M. Functional organization of inferior area 6 in macaque monkey. Exp. Brain Res. 1988, 71, 491–507, doi:10.1007/BF00248742.
Ojemann, G.A. Brain organization for language from the perspective of electrical stimulation mapping. Behav. Brain Sci. 1983, 6, 189–206, doi:10.1017/S0140525X00015491.
[32]
Creutzfeldt, O.; Ojemann, G.; Lettich, E. Single neuron activity in the right and left human temporal lobe during listening and speaking. In Duality and Unity of the Brain; Ottoson, D., Ed.; MacMillan Press: Hampshire, UK, 1987; pp. 295–310. Wenner-Gren International Symposium Series 47.
[33]
Bechtereva, N.P.; Bundzen, P.; Gogolitsin, Y.; Malyshev, V.; Perepelkin, P. Neurophysiological codes of words in subcortical structures of the human Brain. Brain Lang. 1979, 7, 145–163, doi:10.1016/0093-934X(79)90013-0.
[34]
Fries, P.; Nikolic, D.; Singer, W. The gamma cycle. Trends Neurosci. 2007, 30, 309–316, doi:10.1016/j.tins.2007.05.005.
[35]
Ojemann, G.A.; Cawthon, D.F.; Lettich, E. Localization and physiological correlates of language and verbal memory in human lateral temporoparietal cortex. In Neurobiology of Higher Cognitive Function; Scheibel, A.B., Wechsler, A.F., Eds.; Guilford Press: New York, NY, USA, 1990; pp. 185–202.
[36]
Creutzfeldt, O.D.; Ojemann, G.A. University of Washington: Seattle, WA, USA, 1989. Unpublished work.
[37]
Ojemann, G.A.; Schoenfield-McNeill, J.; Corina, D. Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory. Nat. Neurosci. 2002, 5, 64–71, doi:10.1038/nn785.
[38]
Ojemann, G.A.; Schoenfield-McNeill, J.; Corina, D. The Roles of human lateral temporal cortical neuronal activity in recent verbal memory encoding. Cereb. Cortex 2009, 19, 197–205.
[39]
Ojemann, G.A. Organization of short-term verbal memory in language areas of human cortex: Evidence from electrical stimulation. Brain Lang. 1978, 5, 331–340, doi:10.1016/0093-934X(78)90030-5.
[40]
Ojemann, G.A.; Dodrill, C.B. Verbal memory deficits after left temporal lobectomy for epilepsy: Mechanism and intraoperative prediction. J. Neurosurg. 1985, 62, 101–107, doi:10.3171/jns.1985.62.1.0101.
[41]
Zamora, L.; Corina, D.; Schoenfield-McNeill, J.; Lettich, E.; Ojemann, G.; Holmes, M. A comparison of neuronal firing rates for distracted versus non-distracted memory. Soc. Neurosci. Abstr. 2001, 27, 4196.
[42]
Ojemann, G.A.; Schoenfield-McNeill, J.; Corina, D. Different neurons in different regions of human temporal lobe distinguish correct from incorrect identification or memory. Neuropsychologia 2004, 42, 1383–1393, doi:10.1016/j.neuropsychologia.2004.01.008.
[43]
Raichle, M.E.; Fiez, J.; Videen, T.; Prado, J.; Fox, P.; Peterson, S. Practice-related changes in human brain functional anatomy during non-motor learning. Cereb. Cortex 1994, 4, 8–26, doi:10.1093/cercor/4.1.8.
[44]
Ojemann, J.G.; Ojemann, G.A.; Lettich, E. Cortical stimulation mapping of language cortex by using a verb generation task: Effects of learning and comparison to mapping based on object naming. J. Neurosurg. 2002, 97, 33–38, doi:10.3171/jns.2002.97.1.0033.
[45]
Zanos, S.; Zanos, T.; Marmarellis, V.; Ojemann, G.; Fetz, E. Relationship between spike-free local field potentials and spike timing in human temporal cortex. J. Neurophysiol. 2012, 107, 1808–1821, doi:10.1152/jn.00663.2011.
