Overlapping Representation of Primary Tastes in a Defined Region of the Gustatory Cortex

Abstract

Both physiological and imaging approaches have led to often-disparate conclusions about the organization of taste information in gustatory cortex (GC). In this study, we used neuroanatomical and imaging approaches to delineate the likely area of insular cortex given to gustatory function and to characterize taste responses within this delineated area in female and male C57BL/6J mice. Anterograde tracers were injected into the taste thalamus (the medial parvicellular portion of the ventral posterior medial division, VPMpc) of mice and the thalamic terminal field was investigated across the cortex. Working within the delineated area, we used two-photon imaging to measure basic taste responses in Ͼ780 neurons in layer 2/3 located just posterior to the middle cerebral artery. A nonbiased, hierarchical cluster analysis revealed multiple clusters of cells responding best to either individual or combinations of taste stimuli. Taste quality was represented in the activity of taste-responsive cells; however, there was no apparent spatial organization of primary taste qualities in this region.

Single and population coding of taste in the gustatory-cortex of awake mice

“…A total of 185 units were isolated across 10 sessions in 6 mice-4 mice received 2 sessions each (in the latter case sessions were recorded from separate DV locations in the GC; see material and methods). As shown in Figure 1, our recordings spanned much of the region (AP Bregma +1.6 to 0.0; DV 2.25 -3.25 mm from the surface of the brain) receiving input from taste thalamus (Chen et al, 2011;Fletcher et al, 2017) or from the amygdala (Matyas etal., 2014); prior work has shown this region to be important for taste behavior and learning in mice (Neseliler et al, 2011).…”

“…The above data suggest that GC taste neurons are broadly tuned "coarse coders," responding distinctly to multiple tastes; as such, they are consistent with previous reports of taste responses in rat GC (Yamamoto et al, 1985;Bahar et al, 2004;Fontanini and Katz., 2006;Jones et al, 2007;Piette et al, 2012;Samuelsen et al, 2013), and with calcium imaging data from mouse GC (Fletcher et al, 2017; but see Chen et al, 2011).…”

“…As taste is a particularly good sensory system with which to study these three topics (see below and Carleton et al, 2010;Maffei et al, 2012), it is surprising that relatively little work has been done on the electrophysiology of sensory responses within the taste neuroaxis in awake mice. In fact, there has been almost no extensive analysis of central taste electrophysiology in mice (although see Kusamoto-Yoshida et al, 2015): most in vivo assays of murine taste responses come from imaging work, the results of which have been difficult to reconcile with one another (Chen et al, 2011;Fletcher et al, 2017) and with related rat work (which consistently suggests broad responsiveness of regions and individual neurons, see Accolla et al, 2007;Jezzini et al, 2013;Sadacca et al, 2012;Samuelsen & Fontanini, 2017); in particular, it is difficult to analyze fast and subtle neural dynamics (see below) using imaging data.…”

Information-based taste maps in insular cortex are shaped by stimulus concentration

“…Accolla et al, 2007). For instance, Fletcher and colleagues (Fletcher et al, 2017) showed that neurons were preferentially tuned to specific tastes or combination of tastes; nonetheless such neurons were intermingled with neurons tuned to different tastes, in line with the notion of a non-topological gustatory organization in other species (for similar results in non-human primates, see Scott and Plata-Salamán, 1999).…”

“…and colleagues(Fletcher et al, 2017) also observed single taste preferences in the majority of neurons.Considering topological theories, we do not find any evidence for common maps across concentrations, though stable clusters were observed for single concentrations in line with previous research(Chen et al, 2011;Prinster et al, 2017). Moreover, we observed a patchy organization in insular cortex for different taste categories rather than a highly ordered topography(Chen et al, 2011;Prinster et al, 2017).…”