Linking Topography to Tonotopy in the Mouse Auditory Thalamocortical Circuit

Abstract

The mouse sensory neocortex is reported to lack several hallmark features of topographic organization such as ocular dominance and orientation columns in primary visual cortex or fine-scale tonotopy in primary auditory cortex (AI). Here, we re-examined the question of auditory functional topography by aligning ultra-dense receptive field maps from the auditory cortex and thalamus of the mouse in vivo with the neural circuitry contained in the auditory thalamocortical slice in vitro. We observed precisely organized tonotopic maps of best frequency (BF) in the middle layers of AI and the anterior auditory field as well as in the ventral and medial divisions of the medial geniculate body (MGBv and MGBm, respectively). Tracer injections into distinct zones of the BF map in AI retrogradely labeled topographically organized MGBv projections and weaker, mixed projections from MGBm. Stimulating MGBv along the tonotopic axis in the slice produced an orderly shift of voltage-sensitive dye (VSD) signals along the AI tonotopic axis, demonstrating topography in the mouse thalamocortical circuit that is preserved in the slice. However, compared with BF maps of neuronal spiking activity, the topographic order of subthreshold VSD maps was reduced in layer IV and even further degraded in layer II/III. Therefore, the precision of AI topography varies according to the source and layer of the mapping signal. Our findings further bridge the gap between in vivo and in vitro approaches for the detailed cellular study of auditory thalamocortical circuit organization and plasticity in the genetically tractable mouse model.

Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

“…The existence of nonclassical schemes may be in line with findings reported recently: (1) complex FRA maps (Schreiner et al, 2000;Gaese and Ostwald, 2003;Turner et al, 2005); (2) inhibitory sideband effects (O'Connell et al, 2011); (3) high variability along cortical layers (Wallace and Palmer, 2008;Sakata and Harris, 2009;Hackett et al, 2011); and (4) sparseness activation patterns (Hromádka et al, 2008;Sakata and Harris, 2009;Rothschild et al, 2010). Therefore, to study the neuronal substrates for sound attribute codification in A1 of Wistar rats, we chose to apply a simple but complementary approach that is based on a massive exploration of a large cortical sheet at all depths.…”

Cortico‐cortical connectivity within ferret auditory cortex

“…Common principles of cortical organization are also observed in other mammalian species including bats (Esser and Eiermann, 1999; Hoffmann et al, 2008), gerbils (Budinger et al, 2000), guinea pigs (Wallace et al, 2002), rats (Polley et al, 2007; Storace et al, 2010), and mice (Hofstetter and Ehret, 1992; Hackett et al, 2011). Like the ferret, each of these species has a number of tonotopic areas, which are highly interconnected and which receive distinct patterns of thalamic input.…”

Large-scale recording of thalamocortical circuits: in vivo electrophysiology with the two-dimensional electronic depth control silicon probe

“…Because of the tonotopic organization of the rodent auditory thalamocortical system (Hackett et al 2011;Shiramatsu et al 2016) and the features of the EDC probe, we can find regions that are likely connected to each other (Fig. 10).…”