Abstract
The thalamo-cortico-thalamic loop was investigated in adult rats exposed to ethanol during the last week of fetal life. Animals underwent either cortical or thalamic injections of lectin-conjugated horseradish peroxidase. Results demonstrate that prenatal exposure to ethanol causes permanent changes in the thalamocortical circuits. Alterations of thalamo-cortical and cortico-thalamic projections are concentrated at the level of axon terminal fields. The most severe thalamic damage is observed in the anterior intralaminar and midline nuclei; crossed cortico-thalamic projections also appear to be severely impaired. In the cortex, the damage to thalamic terminals displays a medio-lateral gradient of increasing severity through sensori-motor areas, with the lateral fields more impaired. Cells of origin of thalamo-cortical and cortico-thalamic projections are less affected by prenatal ethanol exposure: in the thalamus and layer 5 of sensori-motor cortex labeled cells exhibit normal values of areal numeric density. Conversely, cortico-thalamic neurons of layer 6, especially in the lateral agranular sensori-motor field, display smaller values of areal density than those of normal animals. Possible mechanisms underlying the establishment of these abnormalities are discussed.
Similar content being viewed by others
References
Abel EL, Sokol RJ (1986) Fetal alcohol syndrome is now a leading cause of mental retardation. Lancet 2:1222
Altman J, Bayer SA (1979a) Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. J Comp Neurol 188:455–472
Altman J, Bayer SA (1979b) Development of the diencephalon in the rat. V. Thymidine-radiographic observations on internuclear and intranuclear gradients in the thalamus. J Comp Neurol 188:473–500
Barnes DE, Walker DW (1981) Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Dev Brain Res 1:333–340
Bauer-Moffett CA, Altman J (1977) The effect of ethanol chronically administered to preweanling rats on cerebellar development: a morphological study. Brain Res 119:249–268
Bayer SA, Altman J (1991) Neocortical development. Raven Press, New York
Bonthius DJ, West JR (1990) Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin Exp Res 14:107–118
Cassels B, Wainwright P, Blom K (1987) Heredity and alcohol-induced brain anomalies: effects of alcohol on anomalous prenatal development of the corpus callosum and anterior commissure in BALB/c and C57BL/6 mice. Exp Neurol 95:587–604
Clarren SK, Smith DW (1978) The fetal alcohol syndrome. N Engl J Med 298:1063–1067
Clarren SK, Alvord EC, Sumi SM, Streissguth AP, Smith DW (1978) Brain malformations related to prenatal exposure to ethanol. J Pediatr 92:64–67
Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88
Dow KE, Riopelle RJ (1990) Specific effects of ethanol on neuritepromoting proteoglycans of neuronal origin. Brain Res 508:40–45
Frost DO, Caviness VS Jr (1980) Radial organization of thalamic projections to the neocortex in the mouse. J Comp Neurol 194:369–393
Galofre E, Ferrer I, Fabregues I, Lopez Tejero D (1987) Effects of prenatal ethanol exposure on dendritic spines of layer V pyramidal neurons in the somatosensory cortex of the rat. J Neurol Sci 81:185–195
Gebhardt CA, Naeser MA, Butters N (1984) Computerized measures of CT scans of alcoholics: Thalamic region related to memory. Alcohol 1:133–140
Goldstein DB, Pal N (1971) Alcohol dependence produced in mice by inhalation of ethanol: grading the withdrawal reaction. Science 172:288–290
Graham RC, Karnowsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney in ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302
Hammer RP, Scheibel AB (1981) Morphologic evidence for a delay of neuronal maturation in fetal alcohol exposure. Exp Neurol 74:587–596
Hansson T, Tindberg N, Ingelman Sundberg M, Kohler C (1990) Regional distribution of ethanol-inducible cytochrome P450 IIE1 in the rat central nervous system. Neuroscience 34:451–463
Inomata K, Nasu F, Tanaka H (1987) Decreased density of synaptic formation in the frontal cortex of neonatal rats exposed to ethanol in utero. Int J Dev Neurosci 5:455–460
Ioffe S, Chernick V (1988) Development of the EEG between 30 and 40 weeks of gestation in normal and alcohol-exposed infants. Dev Med Child Neurol 30:797–807
Jones DG (1988) Influence of ethanol on neuronal and synaptic maturation in the central nervous system — Morphological investigations. Prog Neurobiol 31:171–197
Krettek JE, Price JL (1977) The cortical projection of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157–192
Lieber CS, DeCarli LM, Sorrell MF (1989) Experimental methods of ethanol administration. Hepatology 10:501–510
Lindros KO, Väänänen H, Sarviarju M, Haataja H (1984) A simple procedure using 4-methylpyrazole for developing tolerance and other chronic alcohol effects. Alcohol 1:145–150
Magloczky Z, Martos J, Tombol T (1990) Effect of prenatal exposure to ethanol on brains of kittens. I. Changes of neurons in lateral geniculate nucleus. J Hirnforsch 31:761–771
Majchrowicz E (1975) Induction of physical dependence upon ethanol and the associated behavioral changes in rats. Psychopharmacologia (Berl.) 43:245–254
Mankes RF, Glick SD (1986) Preferential alcoholic embryopathy among contiguous siblings of Long-Evans rats. Alcohol Clin Exp Res 10:388–392
Mankes RF, Battles AH, LeFevre R, Hoeven T van der, Glick SD (1992) Preferential alcoholic embryopathy: effects of liquid diets. Lab Anim Sci 42:561–566
McLane JA, Atkinson MB, McNulty J, Breuer AC (1992) Direct measurement of fast axonal organelle transport in chronic ethanol-fed rats. Alcohol Clin Exp Res 16:30–37
Mesulam MM (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 25:106–117
Miller MW (1986) Effects of alcohol on the generation and migration of cerebral cortical neurons. Science 233:1308–1311
Miller MW (1987) Effect of prenatal exposure to alcohol on the distribution and time of origin of cortico-spinal neurons in the rat. J Comp Neurol 257:372–382
Miller MW (1993) Migration of cortical neurons is altered by gestational exposure to ethanol. Alcohol 17:304–314
Miller MW, Dow-Edwards DL (1988) Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol. Brain Res 474:316–326
Miller MW, Potempa G (1990) Numbers of neurons and glia in mature rat somatosensory cortex: effects of prenatal exposure to ethanol. J Comp Neurol 293:92–102
Miller MW, Chiaia NL, Rhoades RW (1990) Intracellular recording and injection study of corticospinal neurons in rat somatosensory cortex: effect of prenatal exposure to ethanol. J Comp Neurol 297:91–105
Minciacchi D, Granato A (1988) Developmental remodeling of thalamic projections to the frontal cortex in rats. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam, pp 501–516
Minciacchi D, Granato A (1989) Development of the thalamocortical system: transient-crossed projections to the frontal cortex in neonatal rats. J Comp Neurol 281:1–12
Minciacchi D, Granato A, Broccolini A, Santarelli M, Sbriccoli A (1991) Foetal alcohol syndrome in the rat: permanent modifications of the thalamo-frontal circuit. Abstracts of the Third IBRO Congress of Neuroscience, Montreal, Canada, August 4–9, p 44
Minciacchi D, Granato A, Santarelli M, Sbriccoli A (1992) Structural changes of thalamo-cortical circuits in a rat foetal alcohol syndrome. Soc Neurosci Abstr 16:423
Minciacchi D, Granato A, Santarelli M, Sbriccoli A (1993) Modifications of thalamo-cortical circuitry in rats prenatally exposed to ethanol. Neuroreport 4:415–418
Molinari M, Minciacchi D, Bentivoglio M, Macchi G (1985) Efferent fibers from the motor cortex terminate bilaterally in the thalamus of rats and cats. Exp Brain Res 57:305–312
Ohnishi K, Lieber CS (1977) Reconstitution of the microsomal ethanol oxidizing system (MEOS): qualitative and quantitative changes of cytochrome P-450 after chronic ethanol consumption. J Biol Chem 252:7124–7131
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, North Ride, Australia
Pierce DR, Goodlett CR, West JR (1989) Differential neuronal loss following early postnatal alcohol exposure. Teratology 40:113–126
Randall CL, Taylor WJ, Walker DW (1977) Ethanol-induced malformations in mice. Alcohol 1:219–224
Smolen AJ, Wright LL, Cunningham TJ (1983) Neuron numbers in the superior cervical sympathetic ganglion of the rat: a critical comparison of methods for cell counting. J Neurocytol 12:739–750
Stoltenburg-Didinger G, Spohr HL (1983) Fetal alcohol syndrome and mental retardation: spine distribution of pyramidal cells in prenatal alcohol-exposed rat cerebral cortex: a Golgi study. Dev Brain Res 11:119–123
Tze WJ, Lee M (1975) Adverse effects of maternal alcohol consumption on pregnancy and fetal growth in rats. Nature 257:479–480
West JR, Goodlett CR (1990) Teratogenic effects of alcohol on brain development. Ann Med 22:319–325
Wise SP, Jones EG (1978) Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178:187–208
Zidenberg-Cherr S, Benak PA, Hurley LS, Keen CL (1988) Altered mineral metabolism: a mechanism underlying the fetal alcohol syndrome in rats. Drug Nutr Interact 5:257–274
Zimmerberg B, Riley EP (1986) Side preference behavior in rats exposed to alcohol prenatally. Neurobehav Toxicol Teratol 8:631–635
Zimmerberg B, Riley EP (1988) Prenatal alcohol exposure alters behavioral laterality of adult offspring in rats. Alcohol Clin Exp Res 12:259–263
Zimmerberg B, Scalzi LV (1989) Commissural size in neonatal rats: effects of sex and prenatal alcohol exposure. Int J Dev Neurosci 7:81–86
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Granato, A., Santarelli, M., Sbriccoli, A. et al. Multifaceted alterations of the thalamo-cortico-thalamic loop in adult rats prenatally exposed to ethanol. Anat Embryol 191, 11–23 (1995). https://doi.org/10.1007/BF00215293
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00215293