A Monosynaptic GABAergic Input from the Inferior Colliculus to the Medial Geniculate Body in Rat

Abstract

The goal was to investigate possible monosynaptic GABAergic projections from the inferior colliculus (IC) to thalamocortical neurons of the medial geniculate body (MGB) in the rat. Although there is little evidence for such a projection in other sensory thalamic nuclei, a GABAergic, ascending auditory projection was reported recently in the cat. In the present study, immunohistochemical and tract-tracing methods were used to identify neurons in the IC that contain GABA and project to the MGB. GABA-positive projection neurons were most numerous in the central nucleus and less so in the dorsal and lateral cortex. They were rare in the lateral tegmental system and brachium of the IC. The dorsal nucleus of the lateral lemniscus also contained GABA-positive projection neurons. In brain slices, stimulation of the brachium produced monosynaptic inhibitory postsynaptic potentials in morphologically identified thalamocortical relay neurons. The inhibitory potentials cannot originate locally, because they persisted when ionotropic glutamatergic transmission was blocked. Typically, brachium stimulation elicited a GABA A -mediated inhibitory potential followed by an excitatory potential and a longer latency GABA Bmediated inhibitory potential.We conclude that the GABA-containing neurons of the IC make short-latency, monosynaptic inputs to the thalamocortical projection neurons in the MGB. Such inputs may distinguish the main auditory pathway from indirect or tegmental auditory pathways as well as from other sensory systems. Monosynaptic inhibitory inputs to the medial geniculate may be important for the regulation of firing patterns in thalamocortical neurons. Key words: auditory pathway; retrograde tracing; brain slice preparation; immunohistochemistry; thalamus; midbrain; reticular formation; dorsal nucleus of the lateral lemniscusRecently, a novel and strong GABA-positive input from the inferior colliculus (IC) has been demonstrated in the cat medial geniculate body (MGB) . Thus, thalamocortical neurons in the MGB may receive monosynaptic, GABA-mediated inputs from the brainstem, in contrast to the neurons of other sensory thalamic nuclei. In most thalamic nuclei, inhibitory inputs come from local interneurons or intrathalamic neurons (for review, see Sherman and Koch, 1986;Steriade and Llinas, 1988). For example, in the lateral geniculate body, ascending inputs can excite directly the interneurons, which in turn inhibit thalamocortical neurons (Hirsch and Burnod, 1987;Lindstrom and Wrobel, 1990;Soltesz and Crunelli, 1992;Pape and McCormick, 1995). Such a scenario is less likely in the rat MGB. There are few local GABAergic interneurons, yet many GABA-positive axonal boutons are present Larue, 1988, 1996). This suggests that inhibitory influences arise outside the MGB. Our goal in this study was to identify and characterize one such inhibitory input in the rat.To test whether thalamocortical neurons of the MGB receive monosynaptic GABAergic input from the lower brainstem, we used both anatomical and electrophysiological...

Organization of projection from brainstem auditory nuclei to the inferior colliculus of Japanese house bat (Pipistrellus abramus)

“…Therefore, it is suggested that LG cells control the entire IC circuit according to global state of brainstem nuclei, while GLU cells control according to the state of specific pathways. LG cells are shown to send long‐range projection to thalamus to elicit inhibitory response faster than excitation (Peruzzi, Bartlett, Smith, & Oliver, 1997). The long‐range connection inside the IC may also cause fast inhibition, which is important for coding complex information such as duration (Casseday et al., 1994).…”

Characterization of Rebound Depolarization in Neurons of the Rat Medial Geniculate Body In Vitro

“…All procedures were approved by the Animal Care and Use Committee at the University of Science and Technology of China. Slices containing the MGB were prepared using a procedure similar to that described previously [21,25]. Briefly, the rat was decapitated and the brain was rapidly removed and submerged in ice-cold artificial cerebrospinal fluid (ACSF) containing (in mmol/L) 129 NaCl, 3 KCl, 1.2 KH 2 PO 4 , 1.3 MgSO 4 , 20 NaHCO 3 , 2.4 CaCl 2 , 3 HEPES, and 10 D-glucose at pH 7.3-7.4 (osmolarity: 300-310 mOsm/ kg).…”

“…In the rat MGB, 99% of the neurons are glutamatergic [14,15] and receive inhibitory inputs mainly from the inferior colliculus and the thalamic reticular nucleus [16][17][18][19][20]. The inhibitory inputs are distributed across the dorsal and ventral parts of the MGB and evoke inhibitory postsynaptic potentials [16,21] which can hyperpolarize an MGB neuron sufficiently to produce a robust RD [22][23][24]. Although RD is a prominent feature of MGB neurons [4,5], its detailed physiological characteristics have not been described.…”

Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

“…Indeed, data from the somatosensory thalamus show that TRN axonal projections display a well-focused terminal field (Pinault and Deschênes 1998). Last, the auditory thalamus of rodent has Ͻ1% of local interneurons Larue 1988, 1996), but the inhibitory inputs coming from the inferior colliculus (Peruzzi et al 1997;Saint Marie et al 1997; can potentially shape the functional properties of MG neurons. More precisely, it is possible that for some MGv cells, the balance between the excitatory and inhibitory inputs coming from the inferior colliculus exerts a major control on the breadth of tuning and threshold.…”

“…The somatosensory thalamus and the auditory thalamus possess 20 -25% of inhibitory interneurons in primate and cat (Benson et al 1991; Fitzpatrick et al 1984;Montero 1989;Penny et al 1983; Spreafrico et al 1983) but Ͻ1% in rat Larue 1988, 1996). In the auditory thalamus (medial geniculate nucleus, MG) of rat and cat, an additional source of GABAergic inhibition is directly provided by the sensory inputs coming from the inferior colliculus (Peruzzi et al 1997;Saint Marie et al 1997;.…”