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

Abstract

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...

Gene Expression Identifies Distinct Ascending Glutamatergic Pathways to Frequency-Organized Auditory Cortex in the Rat Brain

“…Preliminary studies suggest a possible phylogenetic difference and lack of VGLUT1 expression in MGBv of adult primate (Ito and Takada, 2011). The latter may be related to other phylogenetic differences including higher concentrations of inhibitory interneurons in MGBv (Winer et al, 1996;Peruzzi et al, 1997) and higher resolution of frequency responses to sound in cats and primates versus rats (Schreiner et al, 2000;Cheung et al, 2001;Read et al, 2002;Polley et al, 2007). These and many other factors likely contribute to variation in vesicular transporter gene and protein expression patterns during development as well as across species.…”

Effects of Pulse Phase Duration and Location of Stimulation Within the Inferior Colliculus on Auditory Cortical Evoked Potentials in a Guinea Pig Model

“…None of the cases produced any significant trends (P≫0.05) for latency shifts as a function of stimulation location. For more details on the analysis method, see Results: "Latency versus location" 2005) and/or within the medial geniculate nucleus (Winer et al 1996;Peruzzi et al 1997;Bartlett et al 2000;Ito et al 2009;Lee and Sherman 2010) that may not sufficiently respond to the artificially synchronized activation of groups of neurons induced by electrical stimulation. There is some evidence in the cat that greater inhibitory patterns are observed in caudal ICC regions compared to more rostral regions in response to ipsilateral pure tone stimulation based on 2-deoxyglucose mapping (Webster et al 1984).…”

“…Animal studies have demonstrated that projections from the IC to the medial geniculate nucleus are both excitatory and inhibitory (Winer et al 1996;Peruzzi et al 1997;Bartlett et al 2000). Furthermore, the largest tectothalamic neurons are inhibitory (i.e., GABAergic), represent up to 45% (in rat; 20% in cat) of the ascending projections, and provide fast transmission to the medial geniculate nucleus that can precede the excitatory tectothalamic input (Winer et al 1996;Peruzzi et al 1997;Ito et al 2009).…”

Topography and physiology of ascending streams in the auditory tectothalamic pathway

“…Anatomical studies suggest that the inhibitory feedforward projections to the MGB arise throughout the IC (9,10), and physiological investigations find several distinct classes of excitatory and inhibitory inputs (11)(12)(13). However, the topographic organization of excitatory and inhibitory inputs in the tectothalamic pathways is largely undefined.…”