Lateral Hypothalamus Contains Two Types of Palatability-Related Taste Responses with Distinct Dynamics

Abstract

The taste of foods, in particular the palatability of these tastes, exerts a powerful influence on our feeding choices. Although the lateral hypothalamus (LH) has long been known to regulate feeding behavior, taste processing in LH remains relatively understudied. Here, we examined single-unit LH responses in rats subjected to a battery of taste stimuli that differed in both chemical composition and palatability. Like neurons in cortex and amygdala, LH neurons produced a brief epoch of non-specific responses followed by a protracted period of taste-specific firing. Unlike in cortex, however, where palatability-related information only appears 500 ms after the onset of taste-specific firing, taste-specificity in LH was dominated by palatability-related firing, consistent with LH’s role as a feeding center. Upon closer inspection, taste-specific LH neurons fell reliably into one of two subtypes: the first type showed a reliable affinity for palatable tastes, low spontaneous firing rates, phasic responses, and relatively narrow tuning; the second type showed strongest modulation to aversive tastes, high spontaneous firing rates, protracted responses, and broader tuning. Although neurons producing both types of responses were found within the same regions of LH, cross-correlation analyses suggest that they may participate in distinct functional networks. Our data shed light on the implementation of palatability processing both within LH and throughout the taste circuit, and may ultimately have implications for LH’s role in the formation and maintenance of taste preferences and aversions.

Processing of Intraoral Olfactory and Gustatory Signals in the Gustatory Cortex of Awake Rats

“…As measure of the palatability-related activity, we computed a palatability index (Fontanini et al, 2009;Piette et al, 2012;Sadacca et al, 2012;Jezzini et al, 2013;Li et al, 2013;Liu and Fontanini, 2015). This method considers the differences in evoked activity between taste stimuli with similar (sucrose/NaCl, citric acid/quinine) and opposite palatability (sucrose/quinine, NaCl/quinine, sucrose/citric acid, NaCl/citric acid).…”

“…Visual inspection of these plots suggested that responses for bimodal neurons might group by palatability category with responses to palatable tastants being sustained longer than unpalatable ones. To test this possibility, we computed the palatability index ( Jezzini et al, 2013;Li et al, 2013;Liu and Fontanini, 2015) for neurons in the two groups. Briefly, this analysis compares the activity evoked by tastants with similar palatability (i.e., sucrose/NaCl and citric acid/quinine) with activity evoked by hedonically dissimilar tastants (i.e., sucrose/citric acid and sucrose/quinine, etc.…”

“…Electrophysiological recordings have shown that neurons in GC not only encode gustatory stimuli but also process thermal (Kadohisa et al, 2005), visceral (Hanamori et al, 1998 Kusumoto-Yoshida et al, 2015), and orthonasally delivered odors (Vincis and Fontanini, 2016). These multimodal responses are thought to result from anatomical connections between GC and other cortical, thalamic, and limbic areas (Allen et al, 1991;Shi and Cassell, 1998;Haley et al, 2016).…”

“…Human neuroimaging studies have shown that overlapping areas of GC respond to individual presentations of odorants (Savic et al, 2000;Cerf-Ducastel and Murphy, 2001;Poellinger et al, 2001) or tastants (Kobayakawa et al, 1999;Small et al, 1999Small et al, , 2003CerfDucastel et al, 2001;O'Doherty et al, 2001). Additionally, gustatory and olfactory sensory deficits have been observed in patients with GC lesions (Mak et al, 2005).…”

Characterizing the neuropeptide pathways between the forebrain and the pons.

“…Previous electrophysiological studies demonstrate that stimulation or inactivation of the IC, BNST, CeA and LH produces inhibitory and/or excitatory effects on PBN taste cells (Dilorenzo and Monroe, 1992;Li et al, 2005;Li and Cho, 2006;Lundy and Norgren, 2001;Lundy and Norgren, 2004). Thus, CRH and/or Sst forebrain-PBN pathways, in particular those arising from the BNST and CeA, might be involved in mediating these neurophysiological changes thought to play a role in the elaboration of gustatory preference/aversion and, consequently, ingestive behavior (Grossman et al, 2008;Li et al, 2013a;Moran and Katz, 2014;Shimura et al, 1997a;Shimura et al, 1997c;Tokita et al, 2004). Centrally administered CRH and its homologue urocortin have been shown to diminish intake in a variety of species including rodent, while Sst administration augmented intake (Benoit et al, 2000;Fekete et al, 2007;Heinrichs et al, 1993;Jones et al, 1998;Karasawa et al, 2014;Parrott, 1990;Spina et al, 1996;Stengel et al, 2010).…”