Elsevier

Current Opinion in Neurobiology

Volume 40, October 2016, Pages 118-124
Current Opinion in Neurobiology

A gustocentric perspective to understanding primary sensory cortices

https://doi.org/10.1016/j.conb.2016.06.008Get rights and content

Highlights

  • General principles of sensory coding have been derived from neocortical areas.

  • Studying the gustatory cortex (GC) provides a new perspective on sensory processing.

  • GC ensemble activity can be described in terms of metastable dynamics.

  • GC activity is intimately linked to reward processing.

  • GC integrates cross-modal information for the sake of perception and prediction.

Most of the general principles used to explain sensory cortical function have been inferred from experiments performed on neocortical, primary sensory areas. Attempts to apply a neocortical view to the study of the gustatory cortex (GC) have provided only a limited understanding of this area. Failures to conform GC to classical neocortical principles have been implicitly interpreted as a demonstration of GC's uniqueness. Here we propose to take the opposite perspective, dismissing GC's uniqueness and using principles extracted from its study as a lens for looking at neocortical sensory function. In this review, we describe three significant findings related to gustatory cortical function and advocate their relevance for understanding neocortical sensory areas.

Introduction

Historically, sensory physiologists interested in understanding the computations performed by cortical circuits have focused their attention on neocortical areas [1, 2, 3]. The ability to precisely control the physical variables of a stimulus, as well as the ease of experimental access have contributed to rendering visual, somatosensory and auditory cortices primary models for investigating sensory processing. Electrophysiological studies from these areas started earlier and engaged larger communities than studies on chemosensory cortices. As a result, many of the fundamental principles of sensory, cortical physiology have been defined by results obtained in these cortices. The cortical organization in sensory maps [2, 4, 5], the presence of columns [1] and stereotyped circuits [6] and the hierarchical organization of sensory streams (i.e. ‘lower’ order areas devoted to signal processing and ‘higher’ order areas involved in integration) [7] are just few among the many principles established in neocortical areas. Albeit never explicitly theorized, the knowledge accumulated on neocortical areas has influenced the way in which chemosensory areas have been approached. Multiple attempts have been made to adapt general principles of neocortical processing to either olfactory or gustatory cortices [8, 9, 10]. Failures to fit some of such principles to chemosensory areas have been interpreted as evidence for the uniqueness of these cortices. However, many of the results initially deemed as specific to chemosensory cortices have proven to generalize to neocortical areas. For instance, studies of oscillations and their links to sensory coding and cognition have been pioneered in the olfactory system [11, 12, 13, 14]. Similarly, the importance of sensorimotor rhythms has been first established by looking at sniffing and respiration [15, 16, 17, 18]. The recent rise in attention toward the olfactory cortex has brought into focus its relevance for understanding general computational principles. However, a similar process has not yet occurred for the gustatory cortex (GC). In the case of GC, the results have been either viewed as confirmatory of known neocortical principles [8, 9], or, if unique and unprecedented, treated as an exotic peculiarity. In this review, we will discuss recent developments in understanding the function of the gustatory cortex, with the goal of showing how many of the findings on this area can help us gain an original perspective on neocortical sensory areas.

Section snippets

Coding of chemosensory information: the importance of time and dynamics

Neurons in the gustatory cortex are responsible for mediating the perception of different taste qualities: sweet, salty, sour, bitter and umami (just to name the best studied). GC neurons encode chemosensory information via time-varying changes in firing rates [19, 20]. Initial analyses of the time course of firing rate activity revealed a great richness in single neuron responses to intraorally delivered tastants [20]. Most of the firing rate modulations revolved around three temporal epochs

Integration between sensory and reward processing

Taste coding is intimately linked with reward processing. Gustatory stimuli have hedonic valence, they are either palatable or aversive. The reward value of taste can be easily measured relying either on consummatory behaviors [36, 37] or orofacial reactions [38, 39]. The ability to assess objectively different dimensions of reward with specific behavioral tests has allowed researchers in the field to explore the involvement of GC in processing reward. Spatio-temporal patterns of neural

Multisensoriality in a primary sensory cortex

Neurons in GC are not devoted exclusively to processing the physiochemical and affective dimensions of taste. Multiple studies demonstrate that GC can effectively process non-gustatory, cross-modal stimuli encountered either during the consumption of food or even before [19, 46, 49••, 58, 59, 60, 61, 62].

Evidence for multisensory integration during consumption comes from experiments showing that single neurons in GC can encode tactile, thermal and olfactory information coming from the oral

Conclusion

In this brief overview, we discussed three lines of investigation on the function of GC. These approaches have not been directly influenced by existing theories of neocortical sensory function. Rather, these were efforts directed at understanding GC's relationship to gustatory perception and taste-related behaviors. These research directions have contributed to: Firstly, demonstrate that a single computational framework can link sensory coding, sensory-based decisions and spontaneous activity;

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors would like to thank Drs Arianna Maffei, Giancarlo La Camera and Luca Mazzucato for helpful discussions and insightful feedback. RV was funded by Swiss National Science Foundation Fellowships P2GEP3_151816 and P300PA 161021; AF was funded by National Institute of Deafness and Other Communication Disorders Grant R01-DC012543.

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