The insular auditory field receives input from the lemniscal subdivision of the auditory thalamus in mice

Abstract

Here we studied the auditory thalamic input to the insular cortex using mice as a model system. An insular auditory field (IAF) has recently been identified in mice. By using retrograde neuronal tracing, we identified auditory thalamic neurons projecting to the IAF, primary auditory cortex (AI), and anterior auditory field (AAF). After mapping the IAF, AAF, and AI by using optical imaging, we injected a distinct fluorescent tracer into each of the three fields at frequency-matched locations. Tracer injection into the IAF resulted in retrogradely labeled cells localized ventromedially in the lemniscal division, i.e., the ventral subdivision of the medial geniculate body (MGv). Cells retrogradely labeled by injections into the AAF were primarily found in the medial half of the MGv, whereas those from AI injections were located in the lateral half, although some of these two subsets were intermingled within the MGv. Interestingly, retrogradely labeled cells projecting to the IAF showed virtually no overlap with those projecting to the AAF or the AI. Dual tracer injections into two sites responding to low- and high-frequency tones within each of the three auditory fields demonstrated topographic organizations in all three thalamocortical projections. These results indicate that the IAF receives thalamic input from the MGv in a topographic manner, and that the MGv–IAF projection is parallel to the MGv–AAF and MGv–AI projections.

Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation

“…Recent anatomical evidence reveals topographic projections from the auditory thalamus (MGv) directly into the IC (Takemoto et al, 2014). As PV cell-mediated inhibition within the IC matures, activity-dependent pruning of these inputs may be enabled, much as for tonotopic or ocular dominance maps in auditory and visual cortices, respectively (Barkat et al, 2011; Hensch & Stryker, 2004).…”

The auditory corticocollicular system: Molecular and circuit-level considerations

“…With few exceptions (Andersen, Snyder and Merzenich 1980; Budinger et al 2013), most anatomical tracing studies of the CC pathway studies did not involve tonotopic mapping of the AC prior to tracer injection, and therefore tonotopic relationships were inferred based on known maps and the examination of whether changes in injection site produce a systematic change in the location of the tracer in the IC, specifically in the CNIC with its known isofrequency laminae. This point of weakness in the literature will likely improve as optical mapping techniques become more commonly used in conjunction with anatomical tracing (Takemoto et al 2013; Budinger et al 2013). In an early study by Anderson et al in the cat (1980), the investigators systematically injected tracer along the electrophysiologically-characterized tonotopic axis of the AC and found a systematic change in the location of label in the IC.…”

Thalamocortical Projectional Divergence Leads to Complexity in Functional Organizations in Mouse Auditory Cortex

“…The boundary between MGv and MGd can be determined based on immunoreactivity (Lu et al, 2009). Here, we used SMI-32 immunolabeling that strongly stains MGv but not MGd ( Figure 2A) Tsukano et al, 2015), and calbindin immunolabeling that strongly stains MGd but not MGv (Takemoto et al, 2014;Lu et al, 2009). Although some fluorescence-positive neurons were located in MGd as reported previously (Llano and Sherman, 2008), more were found within MGv ( Figure 2B).…”

“…To investigate the origin of thalamic input to A2, we injected retrograde tracers into A2 after regional identification using optical imaging. We triple injected Fast Blue, CTB-488, and CTB-555 (Takemoto et al, 2014) along the tonotopic axis of A2 ( Figures 1E and 1F), prepared consecutive coronal sections, and then visualized fluorescence-positive thalamic neurons.…”

“…Recent tracing studies suggest that the lemniscal thalamocortical pathway is actually composed of several different parallel pathways. Rather than being a single homogenous structure, MGv is composed of multiple compartments, each of which sends frequency-related topological projections to distinct cortical targets Takemoto et al, 2014;Tsukano et al, 2015). At present, the thalamic origins of four cortical tonotopic regions (not including A2) have been identified in rostral and middle parts of MGv (Takemoto et al, 2014;Tsukano et al, 2015).…”