Parvalbumin increases in the medial and lateral geniculate nuclei of aged rhesus macaques

Subcortical auditory structures in the macaque auditory system increase their densities of neurons expressing the calcium binding protein parvalbumin (PV) with age. However, it is unknown whether these increases occur in the thalamic division of the auditory system, the medial geniculate nucleus (MGN). Furthermore, it is also unclear whether these age-related changes are specific to the macaque auditory system or are generalized to other sensory systems. To address these questions, the PV immunoreactivity of the medial and lateral geniculate nuclei (LGN) from seven rhesus macaques ranging in age from 15 to 35 was assessed. Densities of PV expressing neurons in the three subdivisions of the MGN and the six layers of the LGN were calculated separately using unbiased stereological sampling techniques. We found that the ventral and magnocellular subdivisions of the MGN and all six layers of the LGN increased their expressions of PV with age, although increases in the MGN were greater in magnitude than in the LGN. Together, these results suggest that the MGN shows age-related increases in PV expression as is seen throughout the macaque ascending auditory system, and that the analogous region of the visual system shows smaller increases. We conclude that, while there are some similarities between sensory systems, the age-related neurochemical changes seen throughout the macaque auditory system cannot be fully generalized to other sensory systems.

[1]  G. Recanzone,et al.  Age‐related neurochemical changes in the rhesus macaque cochlear nucleus , 2014, The Journal of comparative neurology.

[2]  G. Recanzone,et al.  Age‐related neurochemical changes in the rhesus macaque superior olivary complex , 2014, The Journal of comparative neurology.

[3]  G. Recanzone,et al.  Age-Related Hearing Loss in Rhesus Monkeys Is Correlated with Cochlear Histopathologies , 2013, PloS one.

[4]  H. Adesnik,et al.  A neural circuit for spatial summation in visual cortex , 2012, Nature.

[5]  J. Syka,et al.  Age-related changes in calbindin and calretinin immunoreactivity in the central auditory system of the rat , 2012, Experimental Gerontology.

[6]  Daniel A. Nagode,et al.  Nerve Terminal Nicotinic Acetylcholine Receptors Initiate Quantal GABA Release from Perisomatic Interneurons by Activating Axonal T-Type (Cav3) Ca2+ Channels and Ca2+ Release from Stores , 2011, The Journal of Neuroscience.

[7]  G. Recanzone Perception of auditory signals , 2011, Annals of the New York Academy of Sciences.

[8]  J. Kaas,et al.  Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. , 2009, Cerebral cortex.

[9]  Robert D Frisina,et al.  Age‐related Hearing Loss , 2009, Annals of the New York Academy of Sciences.

[10]  Bevil R. Conway,et al.  Color Vision, Cones, and Color-Coding in the Cortex , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[11]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[12]  M. Furukawa,et al.  Changes in calbindin-D28k and parvalbumin expression in the superior olivary complex following unilateral cochlear ablation in neonatal rats , 2009, Acta oto-laryngologica.

[13]  J. Syka,et al.  Changes in parvalbumin immunoreactivity with aging in the central auditory system of the rat , 2008, Experimental Gerontology.

[14]  Axel Schleicher,et al.  The innervation of parvalbumin‐containing interneurons by VIP‐immunopositive interneurons in the primary somatosensory cortex of the adult rat , 2007, The European journal of neuroscience.

[15]  B. Canlon,et al.  Presbyacusis and calcium-binding protein immunoreactivity in the cochlear nucleus of BALB/c mice , 2006, Hearing Research.

[16]  Lisa A. de la Mothe,et al.  Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[17]  N. Bogdanovic,et al.  Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice , 2004, Neurobiology of Aging.

[18]  E. G. Jones,et al.  Chemically Defined Parallel Pathways in the Monkey Auditory System , 2003, Annals of the New York Academy of Sciences.

[19]  B. Hu Functional organization of lemniscal and nonlemniscal auditory thalamus , 2003, Experimental Brain Research.

[20]  N. Bogdanovic,et al.  Auditory peripheral influences on calcium binding protein immunoreactivity in the cochlear nucleus during aging in the C57BL/6J mouse , 2003, Hearing Research.

[21]  Robert Shapley,et al.  Neural mechanisms for color perception in the primary visual cortex , 2002, Current Opinion in Neurobiology.

[22]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[23]  T. Ono,et al.  Retrospective and prospective coding for predicted reward in the sensory thalamus , 2001, Nature.

[24]  L. Robles,et al.  Mechanics of the mammalian cochlea. , 2001, Physiological reviews.

[25]  M. Soares-Mota,et al.  Nitric oxide synthase‐positive neurons in the rat superior colliculus: Colocalization of NOS with NMDAR1 glutamate receptor, GABA, and parvalbumin , 2001, Journal of neuroscience research.

[26]  A. Graybiel,et al.  Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. , 2001, Journal of neurophysiology.

[27]  P. Kaufman,et al.  Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. , 2000, Archives of ophthalmology.

[28]  P. Hof,et al.  Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns , 1999, Journal of Chemical Neuroanatomy.

[29]  Lotfi B. Merabet,et al.  Motion integration in a thalamic visual nucleus , 1998, Nature.

[30]  P. Morgane,et al.  Comparative analysis of calcium-binding protein-immunoreactive neuronal populations in the auditory and visual systems of the bottlenose dolphin (Tursiops truncatus) and the macaque monkey (Macaca fascicularis) , 1998, Journal of Chemical Neuroanatomy.

[31]  W. O'Neill,et al.  Calbindin D-28k immunoreactivity in the medial nucleus of the trapezoid body declines with age in C57BL/6, but not CBA/CaJ, mice , 1997, Hearing Research.

[32]  W. O'Neill,et al.  Age‐related changes in calbindin D‐28k and calretinin immunoreactivity in the inferior colliculus of CBA/CaJ and C57Bl/6 mice , 1997, The Journal of comparative neurology.

[33]  J. Puel,et al.  Temporary sensory deprivation changes calcium‐binding proteins levels in the auditory brainstem , 1997, The Journal of comparative neurology.

[34]  L. Garey,et al.  NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. , 1996, Cerebral cortex.

[35]  S. Hendry,et al.  Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. , 1996, Cerebral cortex.

[36]  B. B. Lee,et al.  Receptive field structure in the primate retina , 1996, Vision Research.

[37]  A. Hendrickson,et al.  Discrete reduction patterns of parvalbumin and calbindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation , 1994, Visual Neuroscience.

[38]  J. Tigges,et al.  Parvalbumin immunoreactivity in the lateral geniculate nucleus of rhesus monkeys raised under monocular and binocular deprivation conditions , 1993, Visual Neuroscience.

[39]  R. Mize,et al.  Visual deprivation fails to reduce calbindin 28kD or GABA immunoreactivity in the Rhesus monkey superior colliculus , 1992, Visual Neuroscience.

[40]  H. Gundersen,et al.  Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator , 1991, The Anatomical record.

[41]  J. Morrison,et al.  Parvalbumin in the monkey striate cortex: a quantitative immunoelectron-microscopy study , 1991, Brain Research.

[42]  G. Orban,et al.  Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus , 1989, Neuroscience Letters.

[43]  Roger T. Davis,et al.  Behavior and pathology of aging in rhesus monkeys R.T. Davis and C.W. Leathers, Editors. New York: Alan R. Liss, Inc., 1985, 380 pages. ISBN 0-8451-3407-8, LC 85-5251, $88.00 , 1986, Experimental Gerontology.

[44]  R. W. Rodieck,et al.  Analysis of receptive fields of cat retinal ganglion cells. , 1965, Journal of neurophysiology.

[45]  Yoshinao Kajikawa,et al.  Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[46]  H. Vogel,et al.  Calcium-binding proteins. , 2002, Methods in molecular biology.

[47]  A. Aljada,et al.  Nitric oxide synthase. , 1998, Methods in molecular biology.

[48]  D R Moore,et al.  Anatomy and physiology of binaural hearing. , 1991, Audiology : official organ of the International Society of Audiology.

[49]  J. Mollon Color vision. , 1982, Annual review of psychology.

[50]  Leo Maurice Hurvich,et al.  Color vision , 1981 .

[51]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[52]  M. Abercrombie,et al.  Quantitative histology of Wallerian degeneration: I. Nuclear population in rabbit sciatic nerve. , 1946, Journal of anatomy.