Cross‐modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour

Potential auditory compensation in neonatally bilaterally enucleated Syrian hamsters was explored anatomically, electrophysiologically and behaviourally. Gross morphology of the visual cortex appeared normal and no obvious cytoarchitectural malformation was discerned. However, enucleation induced a significant increase in the spontaneous firing rate of visual cortex cells. Further, auditory stimuli elicited field potentials and single unit responses in the visual cortex of enucleated, but not normal, animals. About 63% of the cells isolated in the visual cortex of 16 enucleated hamsters responded to at least one type of auditory stimulus. Most of the responses were less vigorous and less time‐locked than those of auditory cortex cells, and thresholds were typically higher. Projection tracing with WGA–HRP disclosed reciprocal connections between the visual cortex and the dorsal lateral geniculate nucleus in both intact and enucleated animals. However, in the enucleated animals retrogradely labelled cells were also found in the inferior colliculus, the major midbrain auditory nucleus. Behaviourally determined auditory sensitivity across the hearing range did not differ between enucleated and intact hamsters. Minimum audible angle, as determined by a conditioned suppression task, ranged from around 17 to 22°, with no significant difference between normal and enucleated animals. The two groups also did not differ with regard to the direction of their unconditioned head orientating response to intermittent noise. However, the enucleated animals showed a more vigorous response and were slower to habituate to the noise. These results show that bilateral enucleation of newborn hamsters results in auditory activation of visual targets, in addition to the typical activation of the intact auditory pathway. Behaviourally it appears that enucleated hamsters, compared with their normal littermates, are slower to habituate in their response to an unexpected source of sound.

[1]  H. Scheich,et al.  Invasion of visual cortex by the auditory system in the naturally blind mole rat , 1991, Neuroreport.

[2]  S L Pallas,et al.  Cross-modal reorganization of callosal connectivity without altering thalamocortical projections. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  I. Thompson,et al.  Responses of neurons in neonatal cortex and thalamus to patterned visual stimulation through the naturally closed lids. , 2001, Journal of neurophysiology.

[4]  H. Heffner,et al.  Sound localization acuity in the cat: Effect of azimuth, signal duration, and test procedure , 1988, Hearing Research.

[5]  F. Rösler,et al.  Event-related potentials during auditory language processing in congenitally blind and sighted people , 2000, Neuropsychologia.

[6]  Ann M. Graybiel,et al.  The thalamic projection to cortical area 17 in a congenitally anophthalmic mouse strain , 1980, Neuroscience.

[7]  W. Cowan,et al.  Observations on the development of certain ascending inputs to the thalamus in rats. I. Postnatal development. , 1988, Brain research.

[8]  László Négyessy,et al.  Cross‐modal plasticity of the corticothalamic circuits in rats enucleated on the first postnatal day , 2000, The European journal of neuroscience.

[9]  M. Mesulam,et al.  Tracing Neural Connections with Horseradish Peroxidase , 1982 .

[10]  J. Rauschecker,et al.  Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. A. Hoffman,et al.  The golden hamster : its biology and use in medical research , 1968 .

[12]  M. Hallett,et al.  Neural networks for Braille reading by the blind. , 1998 .

[13]  M. Lassonde,et al.  Brain functional reorganization in early blind humans revealed by auditory event‐related potentials , 2000, Neuroreport.

[14]  M. Paré,et al.  Early-blind human subjects localize sound sources better than sighted subjects , 1998, Nature.

[15]  A W Roe,et al.  Visual projections induced into the auditory pathway of ferrets. I. Novel inputs to primary auditory cortex (AI) from the LP/pulvinar complex and the topography of the MGN‐AI projection , 1990, The Journal of comparative neurology.

[16]  O. Smith,et al.  A stereotaxic atlas of the brain of the golden hamster (Mesocricetus auratus) , 1963, The Journal of comparative neurology.

[17]  M. Sur,et al.  Experimentally induced visual projections to the auditory thalamus in ferrets: Evidence for a W cell pathway , 1993, The Journal of comparative neurology.

[18]  D. Frost Axonal growth and target selection during development: retinal projections to the ventrobasal complex and other “nonvisual” structures in neonatal Syrian hamsters , 1984, The Journal of comparative neurology.

[19]  H. Heffner,et al.  Sound localization in chinchillas. I: Left/right discriminations , 1994, Hearing Research.

[20]  J. Rauschecker,et al.  A Positron Emission Tomographic Study of Auditory Localization in the Congenitally Blind , 2000, The Journal of Neuroscience.

[21]  Marta Kutas,et al.  Altered visual-evoked potentials in congenitally deaf adults , 1983, Brain Research.

[22]  R. Näätänen,et al.  Cross-modal reorganization of human cortical functions , 2000, Trends in Neurosciences.

[23]  D. Frost,et al.  Visual responses of neurons in somatosensory cortex of hamsters with experimentally induced retinal projections to somatosensory thalamus. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. R. Michael,et al.  Integration of auditory information in the cat's visual cortex. , 1973, Vision research.

[25]  H. Kennedy,et al.  Characterization of transient cortical projections from auditory, somatosensory, and motor cortices to visual areas 17, 18, and 19 in the kitten , 1988, The Journal of comparative neurology.

[26]  H Summala,et al.  Auditory processing in visual brain areas of the early blind: evidence from event-related potentials. , 1993, Electroencephalography and clinical neurophysiology.

[27]  C. Blakemore,et al.  Functional organization in the visual cortex of the golden hamster , 1976, The Journal of comparative neurology.

[28]  Neonatal enucleation alters functional organization in hamster's lateral posterior nucleus. , 1983, Brain research.

[29]  G. Bronchti,et al.  Retinal projections in the blind mole rat: a WGA-HRP tracing study of a natural degeneration. , 1991, Brain research. Developmental brain research.

[30]  S. Pallas,et al.  Cross-Modal Reorganization of Horizontal Connectivity in Auditory Cortex without Altering Thalamocortical Projections , 1999, The Journal of Neuroscience.

[31]  D. N. Spinelli,et al.  Auditory specificity in unit recordings from cat's visual cortex. , 1968, Experimental neurology.

[32]  Z. Wollberg,et al.  Cross-modal neuroplasticity in the blind mole rat Spalax ehrenbergi: a WGA-HRP tracing study. , 1994, Neuroreport.

[33]  M. Sur,et al.  Visual behaviour mediated by retinal projections directed to the auditory pathway , 2000, Nature.

[34]  A. Volder,et al.  Brain energy metabolism in early blind subjects: neural activity in the visual cortex , 1997, Brain Research.

[35]  J. Rauschecker Compensatory plasticity and sensory substitution in the cerebral cortex , 1995, Trends in Neurosciences.

[36]  H. Heffner,et al.  Audiograms of five species of rodents: implications for the evolution of hearing and the perception of pitch , 2001, Hearing Research.

[37]  N. Hori,et al.  A new method for application of horseradish peroxidase into a restricted area of the brain , 1981, Brain Research Bulletin.

[38]  H. Neville Intermodal Competition and Compensation in Development , 1990, Annals of the New York Academy of Sciences.

[39]  J. Rauschecker,et al.  Auditory Localization Behaviour in Visually Deprived Cats , 1994, The European journal of neuroscience.

[40]  Functional organization of surgically created visual circuits. , 1999, Restorative neurology and neuroscience.

[41]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[42]  M. Hallett,et al.  Period of susceptibility for cross‐modal plasticity in the blind , 1999, Annals of neurology.

[43]  D. Frost,et al.  Surgically created neural pathways mediate visual pattern discrimination. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[45]  M. Sur,et al.  Visual projections induced into the auditory pathway of ferrets: II. Corticocortical connections of primary auditory cortex , 1993, The Journal of comparative neurology.

[46]  W. Crossland,et al.  Neurogenesis in the central visual pathways of the golden hamster. , 1982, Brain research.

[47]  M. Fujii,et al.  Fixation of horseradish peroxidase reaction products with ammonium molybdate , 1984, Neuroscience Research.

[48]  M. Sur,et al.  A map of visual space induced in primary auditory cortex. , 1990, Science.

[49]  R. Ilmoniemi,et al.  Visual cortex activation in blind humans during sound discrimination , 1995, Neuroscience Letters.

[50]  R A Butler,et al.  An analysis of the monaural displacement of sound in space , 1987, Perception & psychophysics.

[51]  R. Mooney,et al.  A substance P projection from the superior colliculus to the parabigeminal nucleus in the rat and hamster , 1989, Brain Research.

[52]  A. Volder,et al.  Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset , 1990, Brain Research.

[53]  C. Asanuma,et al.  Induction of somatic sensory inputs to the lateral geniculate nucleus in congenitally blind mice and in phenotypically normal mice , 1990, Neuroscience.

[54]  O. Fehér,et al.  Neuronal plasticity induced by neonatal monocular (and binocular) enucleation , 1996, Progress in Neurobiology.

[55]  A W Roe,et al.  Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  K Murata,et al.  Neuronal convergence of noxious, acoustic, and visual stimuli in the visual cortex of the cat. , 1965, Journal of neurophysiology.

[57]  R. Rhoades,et al.  Bilateral enucleation alters visual callosal but not corticotectal or corticogeniculate projections in hamster , 1983, Experimental Brain Research.

[58]  H. Kennedy,et al.  Transient projections from the fronto-parietal and temporal cortex to areas 17, 18 and 19 in the kitten , 2004, Experimental Brain Research.

[59]  H. Scheich,et al.  Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. 2‐deoxyglucose study of subcortical centers , 1989, The Journal of comparative neurology.

[60]  FRANK MORRELL,et al.  Visual System's View of Acoustic Space , 1972, Nature.

[61]  U. Yinon,et al.  Pathological and experimentally induced blindness induces auditory activity in the cat primary visual cortex , 2000, Experimental Brain Research.

[62]  M. P. Zwiers,et al.  A Spatial Hearing Deficit in Early-Blind Humans , 2001, The Journal of Neuroscience.

[63]  A J King,et al.  Improved auditory spatial acuity in visually deprived ferrets , 1999, The European journal of neuroscience.

[64]  S. Clarke,et al.  Bilateral transitory projection to visual areas from auditory cortex in kittens. , 1984, Brain research.

[65]  U Yinon,et al.  Auditory activation of cortical visual areas in cats after early visual deprivation , 1999, The European journal of neuroscience.

[66]  M. Sur,et al.  Morphology of retinal axon arbors induced to arborize in a novel target, the medial geniculate nucleus. II. Comparison with axons from the inferior colliculus , 1994, The Journal of comparative neurology.

[67]  M. Moriya,et al.  Auditory projections from the IC to the SCN by way of the LG in the mole, Mogera , 1997, Neuroreport.

[68]  E. Welker,et al.  Barrelfield expansion after neonatal eye removal in mice , 1992, Neuroreport.

[69]  D. Frost,et al.  Induction of functional retinal projections to the somatosensory system , 1985, Nature.

[70]  Alessandra Angelucci,et al.  Induction of visual orientation modules in auditory cortex , 2000, Nature.

[71]  Louis W. Gellermann Chance Orders of Alternating Stimuli in Visual Discrimination Experiments , 1933 .

[72]  A. Smit,et al.  Synapse Formation between Central Neurons Requires Postsynaptic Expression of the MEN1 Tumor Suppressor Gene , 2001, The Journal of Neuroscience.

[73]  L. Deecke,et al.  On the functionality of the visually deprived occipital cortex in early blind persons , 1991, Neuroscience Letters.