Elsevier

Experimental Neurology

Volume 117, Issue 3, September 1992, Pages 230-246
Experimental Neurology

Immunohistochemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentation in the rat visual system

https://doi.org/10.1016/0014-4886(92)90132-AGet rights and content

Abstract

The neuron-specific calcium-binding proteins, parvalbumin and calbindin-D-28k, were studied in the subcortical visual system of normal and unilaterally deafferented albino rats. Immunohistochemistry with monoclonal antibodies was used on vibratome sections through optic tract (OT), dorsal lateral geniculate nucleus (dLGN), olivary pretectal nucleus (OPN), and superior colliculus (SC). In controls, OT stained strongly for parvalbumin and weakly for calbindin-D-28k. The dLGN contained a plexus of parvalbumin-positive fibers. In dLGN, calbindin-D-28k-antibodies showed strong labeling of some neurons with long dendrites and weak staining of the cytoplasm in other neurons. In OPN, parvalbumin stained a ring of neurons and terminals in the shell region, whereas calbindin-D-28k was contained in medial cell populations. In SC, parvalbumin was contained in fibers, terminals, and neurons throughout the visual layer. Calbindin-D-28k showed a laminar distribution of neurons with a predominance in deep portions of superficial grey matter and in ventral portions of stratum opticum. Following unilateral deafferentation induced by optic nerve section, retinal axons showed immunohistochemical changes related to Wallerian degeneration and target neurons reacted by changes of calcium-binding proteins. Parvalbumin and calbindin-D-28k immunostaining decreased during Wallerian degeneration of OT. In the deafferented dLGN, immunohistochemical labeling for calbindin-D-28k declined in strongly stained neurons from 4 to 21 days after lesion. Measurement of dendritic length per number of cells or per area of dLGN showed a significant decline for the contralateral side at 4, 8 and 21 days (ANOVA, P < 0.05). In deafferented OPN, terminal-like staining for parvalbumin decreased and neuronal labeling was enhanced. In deafferented SC, the neuronal and dendritic staining for parvalbumin increased beginning from Day 1 on and persisting at Day 21, whereas fibers and terminal-like elements decreased in staining. Measurement of parvalbumin-positive neurons per area of SC showed a significant increase of labeling in the contralateral side from Day 1 to Day 21 (ANOVA, P < 0.05). These studies show that cellular responses to deafferentation of visual neurons involve a regulation of calcium-binding proteins. The decline in staining for calbindin-D-28k in dLGN may relate to reduced retinal afferent activity. The progressive cellular changes in parvalbumin staining may be related to unmasking of intrinsic neurons after removal of parvalbumin-containing, afferent fibers and terminals. Additionally, the changes of parvalbumin labeling in SC neurons may reflect a plastic reorganization of local circuits known to occur in rat SC in response to deafferentation.

References (95)

  • H. Demeulemeester 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

    Neurosci. Lett.

    (1989)
  • U.T. Eysel et al.

    Increased transneuronal excitation of the cat lateral geniculate nucleus after acute deafferentation

    Brain Res.

    (1978)
  • T.F. Freund

    GABAergic septohippocampal neurons contain parvalbumin

    Brain Res.

    (1989)
  • B. Ghetti et al.

    Transsynaptic response of the lateral geniculate nucleus and the pattern of degeneration of the nerve terminals in the rhesus monkey after eye enucleation

    Brain Res.

    (1972)
  • Y. Ichimiya et al.

    Calbindin-immunoreactive cholinergic neurones in the nucleus basalis of Meynert in Alzheimer-type dementia

    Brain Res.

    (1989)
  • R.-B. Illing et al.

    Parvalbumin in rat superior colliculus

    Neurosci. Lett.

    (1990)
  • F.F. Johansen et al.

    Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia

    Neurosci. Lett.

    (1990)
  • W. Kamphuis et al.

    Kindling induces changes in parvalbumin immunoreactivity in rat hippocampus and its relation to long-term decrease in GABA-immunoreactivity

    Brain Res.

    (1989)
  • T. Kosaka et al.

    GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus

    Brain Res.

    (1987)
  • A.R. Labriola et al.

    Cellular morphology in the visual layer of the developing rat superior colliculus

    Exp. Neurol.

    (1977)
  • D.H. Lowenstein et al.

    Up regulation of calbindin-D28k mRNA in the rat hippocampus following focal stimulation of the perforant path

    Neuron

    (1991)
  • J.S. Lund et al.

    Differential central distribution of optic nerve components in the rat

    Brain Res.

    (1976)
  • S.C. McLoon

    Response of astrocytes in the visual system to Wallerian degeneration: an immunohistochemical analysis of laminin and glial fibrillary acidic protein (GFAP)

    Exp. Neurol.

    (1986)
  • V.M. Montero et al.

    Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradio-graphic study

    Neuroscience

    (1981)
  • L.A. Mudrick et al.

    Long-term structural changes in the rat hippocampal formation following cerebral ischemia

    Brain Res.

    (1989)
  • C. Nitsch et al.

    GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+-binding protein parvalbumin

    Neurosci. Lett.

    (1989)
  • R. Nitsch et al.

    Maintenance of peripheral dendrites of GABAergic neurons requires specific input

    Brain Res.

    (1991)
  • P.T. Ohara et al.

    Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: Immunohistochemical studies by light and electron microscopy

    Neuroscience

    (1983)
  • Y. Okada

    Distribution of γ-aminobutyric acid (GABA) in the layers of the superior colliculus of the rabbit

    Brain Res.

    (1974)
  • S. Okamoto et al.

    Possible induction of (Met)enkephalin-Arg6-Gly7-Leu8 immunoreactivity in neurons of the rat superior colliculus following eye enucleation

    Neurosci. Lett.

    (1990)
  • S. Okamoto et al.

    Contrary effect of eye enucleation on VIP-immunoreactive neurons in the suprachiasmatic nucleus and the superior colliculus of the rat

    Neurosci. Lett.

    (1990)
  • R. Pinard et al.

    Transient increase in [3H]Ro 15-4513 specific binding in the superficial gray layer of the rat superior colliculus induced by visual deafferentation

    Brain Res.

    (1991)
  • B.E. Reese

    The distribution of axons according to diameter in the optic nerve and optic tract of the rat

    Neuroscience

    (1987)
  • B.E. Reese

    The position of the crossed and uncrossed optic axons, and the non-optic axons, in the optic tract of the rat

    Neuroscience

    (1987)
  • B.E. Reese

    Hidden lamination' in the dorsal lateral geniculate nucleus: The functional organization of this thalamic region in the rat

    Brain Res. Rev.

    (1988)
  • W.W. Schlaepfer et al.

    Characterization of the calcium-induced disruption of neurofilaments in rat peripheral nerve

    Brain Res.

    (1979)
  • A. Tokunaga et al.

    Dendritic patterns of neurons in the rat superior colliculus

    Exp. Neurol.

    (1976)
  • M.L. Vizuete et al.

    Effects of enucleation on postnatal development of catecholamines and serotonin metabolism in the superior colliculus of the rat

    Brain Res.

    (1990)
  • F.J. Albers et al.

    Morphometric parameters of the superior colliculus of albino and pigmented rats

    J. Comp. Neurol.

    (1988)
  • A. Bignami et al.

    The fate of axonal debris in Wallerian degeneration of rat optic and sciatic nerves

    J. Neuropathol. Exp. Neurol.

    (1981)
  • G. Campbell et al.

    The olivary pretectal nucleus: Experimental anatomical studies in the rat

    Philos. Trans. R. Soc. London, Ser. B

    (1985)
  • D.A. Carter et al.

    Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters

    J. Neurosci.

    (1989)
  • M.R. Celio

    Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex

    Science

    (1986)
  • M.R. Celio et al.

    Calcium-binding protein parvalbumin as a neuronal marker

    Nature

    (1981)
  • W.M. Cowan

    Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system

  • V. Crunelli et al.

    The ventral and dorsal lateral geniculate nucleus of the rat: Intracellular recordings in vitro

    J. Physiol.

    (1987)
  • V. Crunelli et al.

    A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus

    J. Physiol.

    (1989)
  • Cited by (68)

    • Impact of cochlear ablation on calretinin and synaptophysin in the gerbil anteroventral cochlear nucleus before the hearing onset

      2020, Journal of Chemical Neuroanatomy
      Citation Excerpt :

      Calcium-binding proteins (CaBPs) such a parvalbumin, calbindin-D28k and calretinin (CR) are known intracellular proteins, which have extensively been studied throughout the nervous system in numerous species and therefore considered as selective markers for neurons (Baimbridge et al., 1992; Andressen et al., 1993; Seto-Ohshima, 1994; Celio et al., 1996). In addition, CaBPs respond to a loss of afferent fibers or to the reduction of afferent activity with changes in their expression level or immunohistochemical labeling (Mize and Luo, 1992; Schmidt-Kastner et al., 1992; Heizmann and Braun, 1995; Sans et al., 1995). Interestingly, these proteins are widely distributed throughout the mammalian auditory system (Adams and Mugnaini, 1990; Kelley et al., 1992; Friauf, 1994; Vater and Braun, 1994; Caicedo et al., 1996; Lohmann and Friauf, 1996; Bazwinsky et al., 2003, 2005, 2008, Bazwinsky-Wutschke et al., 2016).

    • Distribution of calcium-binding proteins in the pigeon visual thalamic centers and related pretectal and mesencephalic nuclei. Phylogenetic and functional determinants

      2016, Brain Research
      Citation Excerpt :

      Their neocortical sensory areas seem more similar to the mammalian proisocortex and to the reptilian dorsal cortex, both receiving an input from the relay thalamic nuclei mainly to the superficial cortical layer (Glezer et al., 1998; Hof et al., 1999; Hof and Sherwood, 2005). In the lemniscal (core) of visual (Celio, 1990; Schmidt-Kastner et al., 1992; Luth et al., 1993; Glezer et al., 1998; Jones, 1998; Ishida et al., 2000; Ashwell and Paxinos, 2005; Felch and van Hooser, 2012), and other sensory thalamic centers (Celio, 1990; Braun and Piepenstock, 1993; Jones, 1998, 2003; Martin del Campo et al., 2014) in several nonprimate species, CB-ir neurons prevail on PV-ir neurons (until their disappearance) versus the opposite ratio of these proteins in primates (Jones, 1998). This fact is in favor of the role of the phylogenetic factor in the expression of different CaBPr types.

    • Visual System

      2015, The Rat Nervous System: Fourth Edition
    • Prolonged protein deprivation, but not food restriction, affects parvalbumin-containing interneurons in the dentate gyrus of adult rats

      2013, Brain Research
      Citation Excerpt :

      Interestingly, it has been also reported that PV deficiency reduces seizures threshold and increases the severity of seizures induced by pentylenotetrazol, suggesting that PV also has an important role in the efficient calcium buffering in epilepsy (DeFelipe, 1997; Schwaller et al., 2004; Stern et al., 1974). In other words, the up-regulation of PV in neurons may be interpreted as a survival strategy, reflecting a protective mechanism to counteract the calcium overload (Gomes da Silva et al., 2010; Idrizbegovic et al., 2004; Lister et al., 2011; Schmidt-Kastner et al., 1992) and an attempt to protect the remaining granule and hilar neurons of the dentate gyrus. In the same vein, several other experimental studies have shown that there is an association between the intracellular calcium overload and the increase in PV expression.

    View all citing articles on Scopus
    View full text