Excitatory and inhibitory projections in parallel pathways from the inferior colliculus to the auditory thalamus

Abstract

Individual subdivisions of the medial geniculate body (MG) receive a majority of their ascending inputs from 1 or 2 subdivisions of the inferior colliculus (IC). This establishes parallel pathways that provide a model for understanding auditory projections from the IC through the MG and on to auditory cortex. A striking discovery about the tectothalamic circuit was identification of a substantial GABAergic component. Whether GABAergic projections match the parallel pathway organization has not been examined. We asked whether the parallel pathway concept is reflected in guinea pig tectothalamic pathways and to what degree GABAergic cells contribute to each pathway. We deposited retrograde tracers into individual MG subdivisions (ventral, MGv; medial, MGm; dorsal, MGd; suprageniculate, MGsg) to label tectothalamic cells and used immunochemistry to identify GABAergic cells. The MGv receives most of its IC input (~75%) from the IC central nucleus (ICc); MGd and MGsg receive most of their input (~70%) from IC dorsal cortex (ICd); and MGm receives substantial input from both ICc (~40%) and IC lateral cortex (~40%). Each MG subdivision receives additional input (up to 32%) from non-dominant IC subdivisions, suggesting cross-talk between the pathways. The proportion of GABAergic cells in each pathway depended on the MG subdivision. GABAergic cells formed ~20% of IC inputs to MGv or MGm, ~11% of inputs to MGd, and 4% of inputs to MGsg. Thus, non-GABAergic (i.e., glutamatergic) cells are most numerous in each pathway with GABAergic cells contributing to different extents. Despite smaller numbers of GABAergic cells, their distributions across IC subdivisions mimicked the parallel pathways. Projections outside the dominant pathways suggest opportunities for excitatory and inhibitory crosstalk. The results demonstrate parallel tectothalamic pathways in guinea pigs and suggest numerous opportunities for excitatory and inhibitory interactions within and between pathways.

Differential maturation of vesicular glutamate and GABA transporter expression in the mouse auditory forebrain during the first weeks of hearing

“…These details (discussed below) remain unknown. Most of the GABAergic inputs to the MGB arise from the thalamic reticular nucleus (TRN) and the IC (Bartlett and Smith 1999; Bartlett et al 2000; Geis and Borst 2013; Ito et al 2009, 2011; Mellott et al 2014a, b; Montero and Scott 1983; Peruzzi et al 1997; Winer et al 1996). The TRN neurons receive axon collaterals from both the TC and CT systems of projections, with the exception of the CT axons that originate in L5 (Crabtree 1998; Kimura et al 2005).…”

Evaluation of medial division of the medial geniculate (MGM) and posterior intralaminar nucleus (PIN) inputs to the rat auditory cortex, amygdala, and striatum

“…Unlike cells in MGV/MGD, cells in MGM/PIN receive not only auditory inputs but inputs from other sensory modalities as well. Auditory inputs arise not only from the lemniscal pathway running through the central nucleus of the inferior colliculus (ICC) but a large percentage arises from the nonlemniscal auditory pathway primarily from the external and dorsal cortex of the inferior colliculus (IC; Ledoux, Ruggiero, & Reis, ; Ledoux et al, ; Linke, ; Mellott, Foster, Ohl, & Schofield, ). Synapses from these inputs are both excitatory and inhibitory, terminating primarily on distal dendrites and generating glutamatergic epsps and GABAergic ipsps, respectively (Peruzzi, Bartlett, Smith, & Oliver, ; Smith et al, ; Smith, Bartlett, & Kowalkowski, ).…”

Bilateral projections to the thalamus from individual neurons in the inferior colliculus

“…Finally, the termination pattern of individual tectothalamic axons within each MG is also important, but unknown. Contralateral tectothalamic projections from both GABAergic and glutamatergic cells terminate in each of the three main MG subdivisions (MGd, MGv, MGm; unpublished observations from the same data set described in Mellott, Foster, Ohl, & Schofield, ). It would be of particular interest to identify the termination patterns within each MG for individual bilaterally‐projecting axons; e.g., does a single axon terminate in multiple MG subdivisions?…”

“…We observed bilaterally projecting cells in each of the major subdivisions of the IC. These subdivisions give rise to parallel pathways that have different patterns of termination in the MG and are thought to play different roles in auditory function (see discussion in Mellott, Foster, Ohl, & Schofield, 2014). There is widespread agreement that the subdivisions serve different purposes (Calford & Aitkin, 1983;de Ribaupierre, 1997;Edeline, Manunta, Nodal, & Bajo, 1999;Hu, 2003;Anderson et al, 2007;Abrams, Nicol, Zecker, & Kraus, 2011).…”

“…There may be a third, small population that projects to the contralateral MG and not to the ipsilateral MG (blue circle). Numbers show the maximum values of bilaterally projecting cells as a percentage of cells that project to one or the other MG. Each pathway-ipsilateral, contralateral and bilateral-arises from both GABAergic and non-GABAergic (i.e., glutamatergic) neurons (not shown) [Color figure can be viewed at wileyonlinelibrary.com] tectothalamic projections from both GABAergic and glutamatergic cells terminate in each of the three main MG subdivisions (MGd, MGv, MGm; unpublished observations from the same data set described in Mellott, Foster, Ohl, & Schofield, 2014). It would be of particular interest to identify the termination patterns within each MG for individual bilaterally-projecting axons; e.g., does a single axon terminate in multiple MG subdivisions?…”