Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-21T07:45:55.343Z Has data issue: false hasContentIssue false

Psychophysiological Analysis of the Influence of Vasopressin on Speech in Patients with Post-Stroke Aphasias

Published online by Cambridge University Press:  10 April 2014

Sergei G. Tsikunov*
Affiliation:
Institute for Experimental Medicine, Russian Academy of Medical Sciences, St. Petersburg, Russia
Svetlana G. Belokoskova*
Affiliation:
Institute for Experimental Medicine, Russian Academy of Medical Sciences, St. Petersburg, Russia
*
Correspondence concerning this article should be sent to S.G. Tsikunov, Ph.D. Head of the Laboratory of Psychophysiology of Emotions of NIIEM RAMN. ul. Akad. Pavlova 12, GU NII EM RAMN, St. Petersburg, Russia, 197376: or to S.G. Belokoskova, Ph.D. Researcher, neurologist in the Neurological Clinic of NIIEM RAMN. .E-mail: [email protected]
Correspondence concerning this article should be sent to S.G. Tsikunov, Ph.D. Head of the Laboratory of Psychophysiology of Emotions of NIIEM RAMN. ul. Akad. Pavlova 12, GU NII EM RAMN, St. Petersburg, Russia, 197376: or to S.G. Belokoskova, Ph.D. Researcher, neurologist in the Neurological Clinic of NIIEM RAMN. .E-mail: [email protected]

Abstract

Speech is an attribute of the human species. Central speech disorders following stroke are unique models for the investigation of the organization of speech. Achievements in neurobiology suggest that there are possible neuroendocrine mechanisms involved in the organization of speech. It is known that the neuropeptide vasotocin, analogous of vasopressin in mammals, modulates various components of vocalization in animals. Furthermore, the positive influence of vasopressin on memory, which plays an important role in the formation of speech, has been described. In this study, speech organization processes and their recovery with the administration of vasopressin (1-desamino-8-D-arginin-vasopressin) to 26 patients with chronic aphasias after stroke were investigated. Results showed that sub-endocrine doses of the neuropeptide with intranasal administration had positive influence primarily on simple forms of speech and secondarily on composite forms. There were no statistically significant differences between the sensory and integrative components of the organization of speech processes with vasopressin. In all cases, the positive effect of the neuropeptide was demonstrated. As a result of the effects, speech regulated by both brain hemispheres improved. It is suggested that the neuropeptide optimizes the activity both in the left and right hemispheres, with primary influence on the right hemisphere. The persistence of the acquired effects is explained by an induction of compensatory processes resulting in the reorganization of the intra-central connections by vasopressin.

El habla es un atributo de la especie humana. Los trastornos centrales del habla después de una trombosis cerebral son modelos únicos para la investigación de la organización del habla. Los logros en la neurobiología sugieren que posiblemente haya mecanismos neuroendocrinos implicados en la organización del habla. Se sabe que el neuropéptido vasotocina, análogo de la vasopresina en los mamíferos, modula varios componentes de la vocalización en los animales. Además, se ha descrito la influencia positiva de la vasopresina en la memoria, que juega un papel importante en la formación del habla. En este estudio, se investigaron los procesos de la organización del habla y su recuperación con la administración de la vasopresina (1-desamino-8-D-arginin-vasopressin) a 26 pacientes con afasias crónicas después de una trombosis cerebral. Los resultados mostraron que las dosis sub-endocrinas del neuropéptido con administración intranasal tuvo influencia positiva primariamente en las formas simples del habla y, de manera secundaria, en las formas compuestas. No hubo diferencias estadísticamente significativas entre los componentes sensoriales e integrativos de la organización de los procesos del habla con vasopresina. En todos los casos, se demostró el efecto positivo del neuropéptido. Como resultado de los efectos, mejoró el habla regulado por ambos hemisferios. Se sugiere que el neuropéptido optimiza la actividad tanto en el hemisferio izquierdo como en el derecho, con influencia primaria sobre el hemisferio derecho. La persistencia de los efectos adquiridos se explica por la inducción de procesos compensatorios como resultado de la reorganización de las conexiones intra-centrales por la vasopresina.

Type
Articles
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abo, M., Senoo, A., Watanabe, S., Miyano, S., Doseki, K., Sasaki, N., Kobayashi, K., Kikuchi, Y., & Yonemoto, K. (2004). Language-related brain function during word repetition in poststroke aphasics. Neuroreport, 15, 18911894.CrossRefGoogle Scholar
Balonov, L.I., & Deglin, V.L. (1976). Sluch i rech dominantnogo i subdominantnogo polushari [Hearing and speech of dominant and nondominant hemispheres]. Leningrad, Nauka.Google Scholar
Beeson, P.M., Bayles, K.A., Rubens, A.B., & Kaszniak, A.W. (1993). Memory impairment and executive control in individuals with stroke-induced aphasia. Brain and Language, 45, 253275.CrossRefGoogle ScholarPubMed
Bieser, A., & Muller-Preuss, P. (1996). Auditory responsive cortex in the squirrel monkey: Neural responses to amplitude-modulated sounds. Experimental Brain Research, 108, 273284.CrossRefGoogle ScholarPubMed
Boyd, S.K. (1997). Brain vasotocin pathways and the control of sexual behaviors in the bullfrog. Brain Research Bulletin, 44, 345350.CrossRefGoogle ScholarPubMed
Brinton, R.E., & Gruener, R. (1987). Vasopressin promotes neurite growth in cultures in embryonic neurons. Synapse, 1, 329334.CrossRefGoogle ScholarPubMed
Brudzynski, S.M., Eckersdorf, B., & Golebiewski, H. (1995). Regional specificity of the emotional-aversive response induced by carbachol in the cat brain: A quantitative mapping study. Journal of Psychiatry and Neuroscience, 20, 119132.Google Scholar
Bryden, M. (1982). Laterality (functional asymmetry in the infant brain). NY, LondonGoogle Scholar
Buckner, R.L., Corbetta, M., Schatz, J., Raichle, M.E., & Petersen, S.E. (1996). Preserved speech abilities and compensation following prefrontal damage. Proceedings of the National Academy of Sciences of the United States of America, 93, 12491253.CrossRefGoogle ScholarPubMed
Cappa, S.F., Perani, D., Grassi, F., Bressi, S., Alberoni, M., Franceschi, M., Bettinardi, V., Todde, S., & Fazio, F. (1997). A PET follow-up study of recovery after stroke in acute aphasics. Brain and Language, 56, 5567.CrossRefGoogle ScholarPubMed
Chen, Q., Patel, R., Sales, A., Oji, G., Kim, J., Monreal, A.W., & Brinton, R.D. (2000). Vasopressin-induced neurotrophism in cultured neurons of the cerebral cortex: Dependency on calcium signaling and protein kinase C activity. Neuroscience, 101, 1926.CrossRefGoogle ScholarPubMed
Chertkow, H., Bub, O., Deaudon, C., & Whitehead, V. (1997). On the status of object concepts in aphasia. Brain and Language, 58, 203232.CrossRefGoogle ScholarPubMed
Clark, M. (1994). Communication disorders: What to look for and when to refer. Geriatrics, 49, 5155.Google ScholarPubMed
Dronkers, N.F., Wilkins, D.P., van Valin, R.D. Jr., Redfern, B.B., & Jaeger, J.J. (2004). Lesion analysis of the brain areas involved in language comprehension. Cognition, 92, 145177.CrossRefGoogle ScholarPubMed
Druks, J., & Marshall, J.C. (1995). When passives are easier then actives: Two case studies of aphasic comprehension. Cognition, 55, 311331.CrossRefGoogle ScholarPubMed
Efron, R. (1990). The decline and fall of hemispheric specialization. Hillsdale, NJ: Erlbaum.Google Scholar
Eviatar, Z., Zaidel, E., & Menn, L. (1990). Concreteness: Nouns, verbs and hemispheres. Cortex, 23, 611.CrossRefGoogle Scholar
Fernandez, B., Cardebat, D., Demonet, J.F., Joseph, P.A., Mazaux, J.M., Barat, M., & Allard, M. (2004). Functional MRI followup study of language processes in healthy subjects and during recovery in a case of aphasia. Stroke, 35, 21712176.CrossRefGoogle Scholar
Gazzaniga, M.S. (1995). Consciousness and cerebral hemispheres. The cognitive neurosciences. Cambridge, MA: MIT Press.Google Scholar
Gemba, H., Miki, N., & Sasaki, K. (1997). Cortical field potentials preceding vocalization in monkeys. Acta Oto-Laryngologica, 532(Suppl.), 9698.CrossRefGoogle ScholarPubMed
Ghacibeh, G.A., & Heilman, K.M. (2003). Progressive affective aprosodia and prosoplegia. Neurology, 60, 11921194.CrossRefGoogle ScholarPubMed
Goodal, G. (1984). Morphological complexity and cerebral lateralization. Neuropsychologia, 3, 375380.CrossRefGoogle Scholar
Graham, K.S., Hodges, J.R., & Patterson, K. (1994). The relationship between comprehension and oral reading in progressive fluent aphasia. Neuropsychologia, 32, 299316.CrossRefGoogle ScholarPubMed
Hagoort, P. (1993). Impairment of lexical-semantic processing in aphasia: Evidence from the processing of lexical ambiguities. Brain and Language, 45, 189232.CrossRefGoogle ScholarPubMed
Heilman, K.M., Leon, S.A., & Rosenbek, J.C. (2004). Affective aprosodia from a medial frontal stroke. Brain and Language, 89, 411416.CrossRefGoogle ScholarPubMed
Heiss, W.D., Thiel, A., Kessler, J., Herholz, K. (2003). Disturbance and recovery of language function: Correlates in PET activation studies. Neuroimage, 20, 4249.CrossRefGoogle ScholarPubMed
Josse, G., & Tzourio-Mazoyer, N. (2004). Hemispheric specialization for language. Brain Research Brain Research Review, 44, 112.CrossRefGoogle ScholarPubMed
Karbe, H., Kessler, J., Herhols, K., Fink, G.R., & Heiss, W.D. (1995). Long-term prognosis of poststroke aphasia studied with positron emission tomography. Archives of Neurology, 52, 186190.CrossRefGoogle ScholarPubMed
Kassel, N., & Torner, J. (1984). The International Cooperative Study on timing of aneurism surgery—an update. Stroke, 15, 566670.CrossRefGoogle Scholar
Kerr, J.F.R., Wyllie, A.H., & Currie, A.R. (1972). Apoptosis: A basic biological phenomenon with wide-ranging implication in tissue kinetics. British Journal of Cancer, 26, 239257.CrossRefGoogle ScholarPubMed
Kovacs, G.L., Bohus, B., & Versteed, D.H. (1980). The interaction of posterior pituitary neuropeptides with monoaminergic neurotransmission: Significance in learning and memory processes. Progress of Brain Research, 53, 123140.CrossRefGoogle ScholarPubMed
Lanca, A., Liu, J., Man, H., & Kalant, H. (1995). Peripheral injection of arginine 8-vasopressin increases Fos in specific brain areas. European Journal of Pharmacology, 281, 263269.Google Scholar
Larsen, B., Skinhoj, E., & Lassen, N.A. (1979). Cortical activity of left and right hemisphere provoked by reading and visual naming. A rCBF study. Acta Neurologica Scandinavica, 72 (Suppl.), 6.Google Scholar
Loddenkemper, T., Dinner, D.S., Kubu, C., Prayson, R., Bingaman, W., Dagirmanjian, A., & Wyllie, E. (2004). Aphasia after hemispherectomy in an adult with early onset epilepsy and hemiplegia. Journal of Neurology, Neurosurgery and Psychiatry, 75, 149151.Google Scholar
Luria, A.R. (1970). Traumatic Aphasia. The Hague, Mouton.CrossRefGoogle Scholar
Luria, A.R., & Hutton, G.T. (1977). Modem assessment of the basic forms of aphasia. Brain and Language, 4.Google Scholar
Martin, R.C., & He, T. (2004). Semantic short-term memory and its role in sentence processing: A replication. Brain and Language, 89, 7682.CrossRefGoogle ScholarPubMed
Murphy, K., Corfield, D.R., Guz, A., Fink, G.R., Wise, R.J.S., Harrison, J., & Adams, L. (1997). Cerebral areas associated with motor control of speech in humans. Journal of Applied Physiology, 83, 14381447.CrossRefGoogle ScholarPubMed
Nikiforov, A.S. (1997). Afasia [Aphasia]. Zhurnal Neuropatologii i Psikhiatrii imeni S.S. Korsakova, 9, 5052.Google Scholar
Nikolaenko, N.N., & Egorov, A.Y. (1998). Types of interhemispheric relations in man. Brain and Cognition, 37, 116119.Google Scholar
Nitatori, T. (1995). Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. Journal of Neuroscience, 15, 10011011.CrossRefGoogle ScholarPubMed
Njiokikjien, C., de Sonneville, L., & Vaal, L. (1994). Callosal size in children with learning disabilities. Behavioural Brain Research, 64, 213218.CrossRefGoogle Scholar
Pedersen, P.M., Jorgensen, H.S., Nakayama, H., Raaschou, H.O., & Olsen, T.S. (1995). Aphasia in acute stroke: Incidence, determinants, and recovery. Annals of Neurology, 38, 659666.CrossRefGoogle ScholarPubMed
Perani, D., Cappa, S.F., Tettamanti, M., Rosa, M., Scifo, P., Miozzo, A., Basso, A., & Fazio, F. (2003). A fMRI study of word retrieval in aphasia. Brain and Language, 85, 357368.CrossRefGoogle ScholarPubMed
Radanovic, M., & Scaff, M. (2003). Speech and language disturbances due to subcortical lesions. Brain and Language, 84, 337352.CrossRefGoogle ScholarPubMed
Ronnberg, J., Larsson, C., Fogelsjoo, A., Nilsson, L.G., Lindberg, M., & Angquist, K.A. (1996). Memory dysfunction in mild aphasics. Scandinavian Journal of Psychology, 37, 4661.CrossRefGoogle ScholarPubMed
Saygin, A.P., Wilson, S.M., Dronkers, N.F., & Bates, E. (2004). Action comprehension in aphasia: Linguistic and non-linguistic deficits and their lesion correlates. Neuropsychologia, 42, 17881804.CrossRefGoogle ScholarPubMed
Semmens, J. (1968). Hemispheric specialization: A possible clue to mechanism. Neuropsychologia, 6, 1126.CrossRefGoogle Scholar
Sharp, D.J., Scott, S.K., & Wise, R.J. (2004). Retrieving meaning after temporal lobe infarction: The role of the basal language area. Annals of Neurology, 56, 836846.CrossRefGoogle ScholarPubMed
Sperry, R.H., Gazzaniga, M.S., & Bogen, J.E. (1969). Interhemispheric relationships. The neocortical commissures: Syndromes of hemispheric disconnection. In Vinken, P.J. & Bruyer, G.W. (Eds.), Handbook of clinical neurology, 4, Amsterdam.Google Scholar
Ullman, M.T. (2004). Contributions of memory circuits to language: The declarative/procedural model. Cognition, 92, 231270.CrossRefGoogle ScholarPubMed
Vartanian, G.A., Klementiev, B.I., Neuimina, M.V., & Novikova, T.A. (1994). Neirogumoralnaya induktsia strukturnoi i funktsionalnoi kompensatornoi reorganizatsii povrezshdennogo mozga [Neurohumoral induction of structural and functional compensatory reorganization of the damaged brain]. Vestnik Rossiiyskoy AMN, 1, 2527.Google Scholar
Vartanian, G.A., & Klementiev, B.I. (1991). Himichescaya simmetrya i asimetriya mozqa [The chemical symmetry and asymmetry of the brain]. Leningrad, Nauka, 101128.Google Scholar
Vasserman, L.E., Dorofeeva, S.A., & Meerson, I.A. (1997). Metody neiropsihologicheskoi diagnostiki [Methods of neuropsychological diagnostics]. Saint Petersburg, 15300.Google Scholar
Vawter, M.P., de Wied, D., & van Ree, J.M. (1997). Vasopressin fragment, AVP-(4-8), improves long-term and short-term memory in the whole board search task. Neuropeptides, 31, 489494.CrossRefGoogle Scholar
Vilenski, B.S. (1995). Insult [Stroke]. Saint Petersburg, Medical Informational Agency, 2425.Google Scholar
Voorhuis, Th. A.M., de Kloet, E.R., & de Wied, D. (1988). The distribution and plasticity of (3H) vasopressin labeled specific bindings sites in the canary brain. Brain Research, 457, 148.CrossRefGoogle ScholarPubMed
Ween, J.E., Verfaellie, M., & Alexander, M.P. (1996).Verbal memory function in mild aphasia. Neurology, 47, 795801.CrossRefGoogle ScholarPubMed
Weiller, C., Isensee, C., Rijntjes, M., Huber, W., Muller, S., Bier, D., Dutschka, K., Woods, R.P., Noth, J., & Diener, H.C. (1995). Recovery from Wernicke's aphasia: A positron emission tomographic study. Annals of Neurology, 37, 723732.CrossRefGoogle ScholarPubMed
Wied de, D., Diamant, M., & Fodor, M. (1993). Central nervous system effects of the neurohypophyseal hormones and related peptides. Frontiers in Neuroendocrinology, 14, 251302.CrossRefGoogle Scholar
Winnicka, M.M., & Wisniewski, K. (1998). 6-OHDA bilateral lesions to the nucleus septi lateralis attenuate vasopressin improvement of recall in rats. Pharmacological Research, 37, 145150.CrossRefGoogle Scholar
Wise, R.J. (2003). Language systems in normal and aphasic human subjects: Functional imaging studies and inferences from animal studies. British Medical Bulletin, 65, 95119.CrossRefGoogle ScholarPubMed
Whisnant, J.P., Basford, J. K., & Bernstein, E.F. (1990). Classification of cerebrovascular diseases. Part III. Stroke, 21, 637676.Google Scholar
Wu, P.H., Lanca, A.J., Liu, J.F., Man, C., & Kalant, H. (1995). Peripheral injection of arginin-8-vasopressin increases Fos in specific brain areas. European Journal of Pharmacology, 281, 263269.CrossRefGoogle ScholarPubMed
Xu, X.J., Zhang, M.M., Shang, D.S., Wang, Q.D., Luo, B.Y., & Weng, X.C. (2004). Cortical language activation in aphasia: A functional MRI study. Clinical Medical Journal, 117, 10111016.Google ScholarPubMed
Zahn, R., Drews, E., Specht, K., Kemeny, S., Reith, W., Willmes, K., Schwarz, M., & Huber, W. (2004). Recovery of semantic word processing in global aphasia: A functional MRI study. Brain Research Cognition Brain Research, 18, 322336.CrossRefGoogle ScholarPubMed
Zaidel, E. (1978). Lexical organization in right hemisphere. In Buser, R. & Rougel, P. (Eds.), Cerebral correlates of conscious experience. Elsevier.Google Scholar
Zaidel, E. (1989). Hemispheric independence and interaction in word recognition. Brain and Reading, 54, 77.CrossRefGoogle Scholar