Delta activity encodes taste information in the human brain

Abstract

The categorization of food via sensing nutrients or toxins is crucial to the survival of any organism. On ingestion, rapid responses within the gustatory system are required to identify the oral stimulus to guide immediate behavior (swallowing or expulsion). The way in which the human brain accomplishes this task has so far remained unclear. Using multivariate analysis of 64-channel scalp EEG recordings obtained from 16 volunteers during tasting salty, sweet, sour, or bitter solutions, we found that activity in the delta-frequency range (1-4 Hz; delta power and phase) has information about taste identity in the human brain, with discriminable response patterns at the single-trial level within 130 ms of tasting. Importantly, the latencies of these response patterns predicted the point in time at which participants indicated detection of a taste by pressing a button. Furthermore, taste pattern discrimination was independent of motor-related activation and encoded taste identity rather than other taste features such as intensity and valence. On comparison with our previous findings from a delayed taste-discrimination task (Crouzet et al., 2015), taste-specific neural representations emerged earlier during this speeded taste-detection task, suggesting a goal-dependent flexibility in gustatory response coding. Together, these findings provide the first evidence of a role of delta activity in taste-information coding in humans. Crucially, these neuronal response patterns can be linked to the speed of simple gustatory perceptual decisions - a vital performance index of nutrient sensing.

As Soon as You Taste It: Evidence for Sequential and Parallel Processing of Gustatory Information

“…In conclusion, our results show a close correspondence between the patterns of taste-related psychomotor and the earliest electrophysiological responses, suggesting that behavioral effects are established early in the gustatory processing cascade during stages associated with chemosensory encoding rather than higher-level cognition such as decision making ( Wallroth et al, 2018 ). While detection and discrimination of gustatory stimuli likely occur sequentially, hedonic computations which run in parallel to the purely sensory computations may facilitate taste identification.…”

“…The data were then re-referenced to the average of all electrodes. Finally, we applied zero-phase Hamming-windowed sinc finite impulse response filters (cutoff: −6 dB, maximum passband deviation: 0.2%, stopband attenuation: −53 dB) to isolate the frequency spectrum below 6 ± 2 Hz (order: 330) and above 0.5 ± 1 Hz (order: 660), and subsequently shortened the epochs to −.2 s to 1.5 s. The frequency cutoff was based on recent findings showing that taste quality information is encoded within the power and phase information of the δ and lower θ frequency bands (roughly up to 6 Hz; Hardikar et al, 2018 ; Wallroth et al, 2018 ; see also Pavao et al, 2014 ). Trials were then normalized by subtracting the average of each electrode’s baseline period (−200 ms to stimulus onset) before decoding analysis.…”

“…Given previous findings that taste qualities can be successfully decoded from EEG recordings (cf. Crouzet et al, 2015 ; Hardikar et al, 2018 ; Wallroth et al, 2018 ), our chief concern was to find an adjustment procedure which balances Type I and Type II error rates such that we would identify the taste-signal onset as accurately as possible (i.e., with a minimal number of false alarms but also as few misses of the true signal). To summarize, our present motivation was to explore exactly when a taste-signal emerges at the single-trial level, rather than to investigate whether a taste-signal occurs at all.…”

“…Each taste category is detected by specific receptors, mostly on the tongue ( Roper and Chaudhari, 2017 ), and taste-specific information is transduced to the brainstem, eventually arriving at dissociable cortical representations ( Katz et al, 2002 ; Schoenfeld et al, 2004 ; Pavao et al, 2014 ; Crouzet et al, 2015 ; Wallroth et al, 2018 ). Despite detailed descriptions of peripheral and central sites of gustatory information processing, the emergence of the taste processing cascade, such as the detection of and discrimination between tastes, is not yet understood.…”

Event-Related Brain Potentials Associated With the Olfactory-Visual Stroop Effect and Its Modulation by Olfactory-Induced Emotional States

“…Unlike other sensory channels (e.g., vision, audition, or touch), bottom-up afferences from the olfactory receptors bypass the thalamic "first-order" relay neurons and directly influence a region of the olfactory (piriform) cortex (Gottfried and Zald, 2005). The speed of olfactory information far exceeds that of taste (Szyszka et al, 2012;Wallroth et al, 2018). Thus, one simple explanation for this earlier peak observed in the current study could be that the speed of olfactory information processing is faster than that of taste.…”