Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus

Marie, Richard L. Saint; Benson, Christina G.; Ostapoff, E.-Michael; Morest, D. Kent

doi:10.1016/0378-5955(91)90003-r

Cited by 140 publications

(102 citation statements)

References 49 publications

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“…These cells are probably glycinergic and project to the DCN (Smith and Rhode, 1989), and therefore they are a likely source of the short-latency inhibition to type II and IIIϩIV cells. A common source of inhibition that is strong to type II and weaker to IIIϩIV cells was suggested earlier (Nelken and Young, 1994), and is consistent with results from electrical stimulation of the auditory nerve (Shofner and Young, 1985;O'Leary et al, 1994) and with numerous previous studies (Smith and Rhode, 1985;Caspary et al, 1987;Snyder and Leake, 1988;Oertel et al, 1990;Saint Marie et al, 1991;Evans and Zhao, 1993;Zhang andOertel, 1993, 1994).…”

Section: Temporal Propertiessupporting

confidence: 76%

Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract

Joris

Smith

1998

J. Neurosci.

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The dorsal cochlear nucleus (DCN) is one of three nuclei at the terminal zone of the auditory nerve. Axons of its projection neurons course via the dorsal acoustic stria (DAS) to the inferior colliculus (IC), where their signals are integrated with inputs from various other sources. The DCN presumably conveys sensitivity to spectral features, and it has been hypothesized that it plays a role in sound localization based on pinna cues. To account for its remarkable spectral properties, a DCN circuit scheme was developed in which three inputs converge onto projection neurons: auditory nerve fibers, inhibitory interneurons, and wide-band inhibitors, which possibly consist of Onset-chopper (O c ) cells. We studied temporal and binaural properties in DCN and DAS and examined whether the temporal properties are consistent with the model circuit.Interneurons (type II) and projection (types III and IV) neurons differed from O c cells by their longer latencies and temporally nonlinear responses to amplitude-modulated tones. They also showed evidence of early inhibition to clicks. All projection neurons examined were inhibited by stimulation of the contralateral ear, particularly by broadband noise, and this inhibition also had short latency. Because O c cells had shortlatency responses and were well driven by broadband stimuli, we propose that they provide short-latency inhibition to DCN for both ipsilateral and contralateral stimuli. These results indicate more complex temporal behavior in DCN than has previously been emphasized, but they are consistent with the recently described nonlinear behavior to spectral manipulations and with the connectivity scheme deduced from such manipulations. Key words: audition; dorsal cochlear nucleus; dorsal acoustic stria; amplitude modulation; temporal; binaural; catThe dorsal cochlear nucleus (DC N) is one of three nuclei at the terminal zone of the auditory nerve. Axons of its projection cells leave the nucleus via the dorsal acoustic stria (DAS) and project to the inferior colliculus (IC) (Osen, 1972;Adams and Warr, 1976;Oliver, 1984). The DC N is the most complex subdivision of the cochlear nucleus, and its f unction remains unknown. Young and colleagues (1992) proposed that the DC N serves a role in the detection of spatial elevation of a sound source by virtue of its sensitivity to spectral features such as those resulting from the directionally dependent filtering properties of the pinna.One strategy for obtaining clues to the f unction of the DCN is to examine the effect of its very nonlinear spectral properties (Nelken et al., 1997) on the IC (Semple and Aitkin, 1980). For example, inputs from the DC N partly converge with inputs from the lateral superior olive (L SO) (Oliver et al., 1997). C ells in the LSO are sensitive to interaural level differences (ILDs) (Boudreau and Tsuchitani, 1968) and interaural time differences of amplitude-modulated (AM) tones , which are cues to the azimuthal position of a sound source. C ells in the IC with spatially restricted receptive fields...

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Section: Temporal Propertiessupporting

confidence: 76%

Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract

Joris

Smith

1998

J. Neurosci.

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“…Perhaps the definition of a local circuit neuron should be enlarged to include GABAergic cells with both intrinsic and remote projections. A second conclusion is that the feedforward inhibition so prevalent in the auditory brain stem (31)(32)(33) is also found in the TT pathway.…”

Section: Discussionmentioning

confidence: 93%

GABAergic feedforward projections from the inferior colliculus to the medial geniculate body.

Winer

Marie

Larue

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

165

111

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A novel and robust projection from y-aminobutyric acid-containing (GABAergic) inferior colliculus neurons to the medial geniculate body (MGB) was discovered in the cat using axoplasmic transport methods combined with immunocytochemistry. This input travels with the classical inferior colliculus projection to the MGB, and it is a direct ascending GABAergic pathway to the sensory thalamus that may be inhibitory. This bilateral projection constitutes 10-30% of the neurons in the auditory tectothalamic system. Studies by others have shown that comparable input to the corresponding thalamic visual or somesthetic nuclei is absent. This suggests that monosynaptic inhibition or disinhibition is a prominent feature in the MGB and that differences in neural circuitry distinguish it from its thalamic visual and somesthetic counterparts.The thalamus is the gateway controlling the flow of sensory information reaching the cerebral cortex (1). The consensus is that input ascending to the primary thalamic nuclei for hearing (2), vision (3), and somesthesis (4) is entirely excitatory. We describe here a prominent and unexpected projection from y-aminobutyric acid-containing (GABAergic) cells in the inferior colliculus (IC) to the medial geniculate body (MGB) in the auditory tectothalamic (TT) pathway that constitutes an exception to this principle. This suggests that there is a convergence of classical excitatory and putatively inhibitory projections within the MGB and that an ascending pathway considered as neurochemically unitary in fact contains more than one channel. This striking difference in feedforward input between the auditory thalamus and other thalamic sensory nuclei is surprising since each has similar structural and intrinsic features (5-7), shared physiological properties (8-10), analogous cortical projection patterns (11-13), and a closely related neurochemical organization (14, 15). The present results suggest that, despite these parallels, there must be differences in circuitry and information processing regimes within the sensory thalamus.with isoflurane at a level that suppressed all nociceptive reflexes. All experimental procedures followed the applicable and approved institutional animal care and use protocols. Four unilateral penetrations were made using stereotaxic coordinates to target specific nuclei in various subdivisions. A total of seven, 50-nl deposits were made at 500-,um intervals along a track with a glass micropipet; the net volume was -1.5 ,lI.The animal was reanesthetized 3 days later and perfused with PBS followed by 2% paraformaldehyde and 3% glutaraldehyde in 0.12 M PB. Vibratome sections, 50-,m-thick, were collected in 0.1 M PB and placed in blocking serum (5% normal goat serum) for 60 min. Tissue was incubated overnight at 4°C in rabbit-anti-GABA (Incstar, Stillwater, MN) diluted 1:5000 and then reacted using avidin-biotin immunoperoxidase (Vectastain, Vector Laboratories, Burlingame, CA) with diaminobenzidine as the chromagen. WAHG labeling was intensified with silver (IntenSE-M...

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“…One major source of glycinergic inhibition arises from vertical cells, which inhibit responses to narrow-band stimuli Young, 1980, 1990;Caspary et al, 1987;Saint-Marie et al, 1991;Spirou et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…DCN neurons, including fusiform, giant, and vertical cells, receive primary afferent excitatory inputs from acoustic nerve fibers as well as intrinsic and extrinsic inputs from auditory and nonauditory sources (Cant and Benson, 2003;Arnott et al, 2004;Young and Oertel, 2004;Zhou and Shore, 2004). DCN output neurons, especially fusiform cells, receive focused glycinergic input from tonotopically aligned vertical cells (Rhode, 1999) and less frequency-focused inhibitory inputs from glycinergic D-multipolar cells in the ventral cochlear nucleus (Saint-Marie et al, 1991;Kolston et al, 1992: Doucet et al, 1999. Vertical cells, termed narrow-band inhibitors, project strong nearcharacteristic frequency (CF) glycinergic inhibition onto fusiform cells (Caspary et al, 1987;Rhode, 1999;Davis and Young, 2000).…”

Section: Introductionmentioning

confidence: 99%

Age-Related Changes in the Inhibitory Response Properties of Dorsal Cochlear Nucleus Output Neurons: Role of Inhibitory Inputs

Caspary

Schatteman²,

Hughes³

2005

J. Neurosci.

156

114

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Age-related hearing loss frequently results in a loss in the ability to discriminate speech signals, especially in noise. This is attributable, in part, to a loss in temporal resolving power and ability to adjust dynamic range. Circuits in the adult dorsal cochlear nucleus (DCN) have been shown to preserve signal in background noise. Fusiform cells, major DCN output neurons, receive focused glycinergic inputs from tonotopically aligned vertical cells that also project to the ventral cochlear nucleus. Glycine-mediated inhibition onto fusiform cells results in decreased tone-evoked activity as intensity is increased at frequencies adjacent to characteristic frequency (CF). DCN output is thus shaped by glycinergic inhibition, which can be readily assessed in recordings from fusiform cells. Previous DCN studies suggest an age-related loss of markers for glycinergic neurotransmission. The present study postulated that response properties of aged fusiform cells would show a loss of inhibition, resembling conditions observed with glycine receptor blockade. The functional impact of aging was examined by comparing response properties from units meeting fusiform-cell criteria in young and aged rats. Fusiform cells in aged animals displayed significantly higher maximum discharge rates to CF tones than those recorded from young-adult animals. Fusiform cells of aged rats displayed significantly fewer nonmonotonic CF rate-level functions and an age-related change in temporal response properties. These findings are consistent with an age-related loss of glycinergic input, likely from vertical cells, and with findings from other sensory aging studies suggesting a selective age-related decrement in inhibitory amino acid neurotransmitter function.

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Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus

Cited by 140 publications

References 49 publications

Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract

Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract

GABAergic feedforward projections from the inferior colliculus to the medial geniculate body.

Age-Related Changes in the Inhibitory Response Properties of Dorsal Cochlear Nucleus Output Neurons: Role of Inhibitory Inputs

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