Skip to main content
SpringerLink
Log in

Multisensory Processing of Gustatory Stimuli

  • Published:
Chemosensory Perception

Abstract

The brain’s processing of gustatory stimuli is inherently multimodal, since at approximately the same time that intraoral stimuli activate receptors on taste cells, somatosensory information is concurrently conveyed to the central nervous system. We first present evidence that throughout the oral cavity, often a single chemical stimulus will concomitantly activate different receptors expressed on taste cells and somatosensory nerve terminals. We then argue that gustatory perception is intrinsically linked to concurrent somatosensory processing. Finally, we review evidence showing that central gustatory pathways are sites where multisensory integration occurs, with particular emphasis on somatosensory responses in the gustatory cortex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. We do not consider olfactory stimuli in this report. We note that the gustatory pathways may also have thermal and mechanical sensitivity and, as described below, the somatosensory system is responsive to chemical stimuli, but its response may be slower than for the taste pathway.

  2. The precise NaCl concentration that a rat will find aversive will depend on many factors including its state of hydration, strain, and body sodium levels. As a rule of thumb, animals begin to find NaCl aversive when the solutions become hypertonic but are clearly aversive at 0.3 M. For example, see Fregly (1996) and Fregly and Rowland (1992).

  3. It has been recently suggested that the entire cortex is multisensory (Ghazanfar and Schroeder 2006).

References

  • Boucher Y, Simons CT, Faurion A, Azerad J, Carstens E (2003a) Trigeminal modulation of gustatory neurons in the nucleus of the solitary tract. Brain Res 973:265–274

    Article  CAS  Google Scholar 

  • Boucher Y, Simons CT, Faurion A, Azerad J, Carstens E (2003b) Trigeminal modulation of gustatory neurons in the nucleus of the solitary tract. Brain Res 973:265–274

    Article  CAS  Google Scholar 

  • Breslin PA, Huang L (2006) Human taste: peripheral anatomy, taste transduction, and coding. Adv Otorhinolaryngol 63:152–190

    Google Scholar 

  • Burnette RR (1984) A Monte-Carlo model for the passive diffusion of drugs across the stratum corneum. Int J Pharm 22:89–97

    Article  CAS  Google Scholar 

  • Carstens E, Kuenzler N, Handwerker KO (1998) Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to the oral or ocular mucosa. J Neurophysiol 80:465–492

    CAS  Google Scholar 

  • Carstens E, Albin KC, Simons CT, Carstens MI (2007) Time course of self-desensitization of oral irritation by nicotine and capsaicin. Chem Senses 32:811–816

    Article  CAS  Google Scholar 

  • Cerf-Ducastel B, van de Moortele PF, MacLeod P, Le Bihan D, Faurion A (2001) Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic image study. Chem Senses 26:371–383

    Article  CAS  Google Scholar 

  • Chrandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zucker CS, Ryba NJP (2000) T2Rs function as bitter taste receptors. Cell 100:703–711

    Article  Google Scholar 

  • Cliff MA, Green BG (1996) Sensitization and desensitization to capsaicin and menthol in the oral cavity: interactions and individual differences. Physiol Behav 59:487–494

    Article  CAS  Google Scholar 

  • Costa RM, Liu L, Nicolelis MAL, Simon SA (2004) Gustatory effects of capsaicin that are independent of TRPV1 receptors. Chem Senses 30:i198–i200

    Article  CAS  Google Scholar 

  • Dahl M, Erickson RP, Simon SA (1997) Neural responses to bitter compounds in the rat. Brain Res 756:22–34

    Article  CAS  Google Scholar 

  • de Araujo IET, Kringelbach ML, Rolls ET, McGlone F (2003) Human cortical responses to water in the mouth and the effects of thirst. J Neurophysiol 90:1865–1876

    Article  Google Scholar 

  • Fregly MJ (1996) On the spontaneous intake of NaCl solution by dogs. In: Kare MR, Fregly MJ, Bernard RA (eds) Biological and behavioral aspects of salt intake. Academic, New York, pp 55–68

    Google Scholar 

  • Fregly MJ, Rowland NE (1992) Comparison of preference thresholds for NaCl solution in rats of the Sprague–Dawley and Long–Evans strains. Physiol Behav 51:915–918

    Article  CAS  Google Scholar 

  • Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278–285

    Article  Google Scholar 

  • Green BG, Gelhard B (1989) Salt as an oral irritant. Chem Senses 14:259–271

    Article  CAS  Google Scholar 

  • Halpern BP, Tapper DN (1971) Taste stimuli: quality coding time. Science 171:1256–1258

    Article  CAS  Google Scholar 

  • Hanamori T, Kunitake T, Kato K, Kannan H (1997) Convergence of afferent inputs from the chorda tympani, lingual–tonsillar and pharyngeal branches of the glossopharyngeal nerve, and superior laryngeal nerve on the neurons in the insular cortex in rats. Brain Res 763:267–270

    Article  CAS  Google Scholar 

  • Hanamori T, Kunitake T, Kato K, Kannan H (1998) Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J Neurophysiol 79:2535–2545

    CAS  Google Scholar 

  • Holzer P (1988) Local effector functions of capsaicin-sensitive nerve endings: involvement of tachykinins. Neuroscience 24:739–768

    Article  CAS  Google Scholar 

  • Kadohisa M, Rolls ET, Verhagen JV (2004) Orbitofrontal cortex: neuronal representation of oral temperature and capsaicin in addition to taste and texture. Neuroscience 127:207–221

    Article  CAS  Google Scholar 

  • Kadohisa M, Verhagen JV, Rolls ET (2005) The primate amygdala: neuronal representations of the viscosity, fat texture, temperature, grittiness and taste of foods. Neuroscience 132:33–48

    Article  CAS  Google Scholar 

  • Katz DB, Simon SA, Nicolelis MAL (2001) Dynamic and multimodal response of gustatory cortical neurons. J Neurosci 21:4478–4489

    CAS  Google Scholar 

  • Kawamura Y, Okamoto J, Funakoshi M (1968) A role of oral afferents in aversion to taste solutions. Physiol Behav 3:537–542

    Article  CAS  Google Scholar 

  • Laurienti PJ, Perrault TJ, Stanford TR, Wallace MT, Stein BE (2005) On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies. Exp Brain Res 166:289–297

    Article  Google Scholar 

  • Lemon CH, Smith DV (2005) Neural representation of bitter taste in the nucleus of the solitary tract. J Neurophysiol 94:3719–3729

    Article  CAS  Google Scholar 

  • Lim J, Green BG (2007) The psychophysical relationship between bitter taste and burning sensation: evidence of qualitative similarity. Chem Senses 32:31–39

    Article  Google Scholar 

  • Liu L, Simon SA (1996) Capsaicin and nicotine both activate a subset of rat trigeminal ganglion neurons. Am J Physiol 270(Pt 1):C1807–C1814

    CAS  Google Scholar 

  • Liu L, Simon SA (2000) Capsaicin, acid and heat evoked currents in rat trigeminal ganglion neurons: evidence for functional VR1 receptors. Physiol Behav 69:363–378

    Article  CAS  Google Scholar 

  • Liu L, Chang G-Q, Jiao Y, Simon SA (1998) Neuronal nicotinic acetylcholine receptors in rat trigeminal ganglia. Brain Res 809:238–245

    Article  CAS  Google Scholar 

  • Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA (2004) Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 91:1482–1491

    Article  CAS  Google Scholar 

  • Lundbaek JA, Birn P, Tape SE, Toombes GES, Sogaard R, Koeppe RE II, Gruner SM, Hansen AJ, Andersen OS (2005) Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. Mol Pharmacol 68:680–689

    CAS  Google Scholar 

  • Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, DeSimone JA (2004) The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol (Lond) 558:147–159

    Article  CAS  Google Scholar 

  • Lyall V, Heck GL, Phan TH, Mummalaneni S, Malik SA, Vinnikova AK, DeSimone JA (2005) Ethanol modulates the VR-1 variant amiloride-insensitive salt taste receptor. ii. Effect on chorda tympani salt responses. J Gen Physiol 125:587–600

    Article  CAS  Google Scholar 

  • Lyall V, Phan TH, Mummalaneni S, Mansouri M, Heck GL, Kobal G, DeSimone JA (2007) Effect of nicotine on chorda tympani responses to salty and sour stimuli. J Neurophysiol 98:1662–1674

    Article  CAS  Google Scholar 

  • Mistretta CM (1971) Permeability of tongue epithelium and its relation to taste. Am J Physiol 220:1162–1167

    CAS  Google Scholar 

  • Norgren R (1995) Gustatory system. In: Paxinos G (ed) The rat nervous system. Academic, San Diego, pp 751–771

    Google Scholar 

  • Ogawa H, Ifuku H, Nakamura T, Hirata S (2005) Possible changes in information from the primary to higher-order gustatory cortices, studied by recording neural activities during a taste discrimination GO/NOGO task in monkeys. Chem Senses 30:78–79

    Article  Google Scholar 

  • Okuni Y (1977) Response of chorda tympani fibers of the rat to pungent spices and irritants in pungent spices. Shikwa Gakuho 77:1323–1349

    CAS  Google Scholar 

  • Pfaffmann C, Bartoshuk L, McBurney DH (1971) Taste psychophysics. In: Beidler LM (ed) Handbook of sensory physiology. Springer, New York, pp 76–98

    Google Scholar 

  • Riera CE, Vogel H, Simon SA, Coutre J1 (2007) Artificial sweeteners and salts producing a metallic taste sensation activate TRPV1 receptors. Am J Physiol Regul Integr Comp Physiol 293:R626–R634

    CAS  Google Scholar 

  • Rolls ET, Baylis LL (1994) Gustatory, olfactory and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5442

    CAS  Google Scholar 

  • Ruiz C, Gutknecht S, Delay E, Kinnamon S (2006) Detection of NaCl and KCl in TRPV1 knockout mice. Chem Senses 31:813–820

    Article  CAS  Google Scholar 

  • Scott TR, Mark GP (1987) The taste system encodes toxicity. Brain Res 414:197–203

    Article  CAS  Google Scholar 

  • Scott TR, Plata-Salaman CR (2003) Taste in the monkey cortex. Physiol Behav 67:489–511

    Article  Google Scholar 

  • Shepherd GM (2006) Smell images and the flavour system in the human brain. Nature 444:316–321

    Article  CAS  Google Scholar 

  • Simon SA, Liu L, Erickson RP (2003) Neuropeptides modulate rat chorda tympani responses. Am J Physiol Regul Integr Comp Physiol 284:R1494–R1505

    CAS  Google Scholar 

  • Simon SA, de Araujo IE, Gutierrez R, Nicolelis MAL (2006) The neural mechanisms of gustation: a distributed processing code. Nat Rev Neurosci 7:890–901

    Article  CAS  Google Scholar 

  • Simons CT, Sudo S, Sudo M, Carstens E (2003) Mecamylamine reduces nicotine cross-desensitization of trigeminal caudalis neuronal responses to oral chemical irritation. Brain Res 991:249–253

    Article  CAS  Google Scholar 

  • Simons CT, Boucher Y, Carstens MI, Carstens E (2006) Nicotine suppression of gustatory responses of neurons in the nucleus of the solitary tract. J Neurophysiol 96:1877–1886

    Article  CAS  Google Scholar 

  • Squier CA (1973) The permeability of keratinized and nonkeratinized oral epithelium to horseradish peroxidase. J Ultrastruct Res 43:160–177

    Article  CAS  Google Scholar 

  • Squier CA, Johnson NW (1975) Permeability of oral muscosa. Br Med Bull 31:169–175

    CAS  Google Scholar 

  • Stanford TR, Stein BE (2007) Superadditivity in multisensory integration: putting the computation in context. Neuroreport 18:787–792

    Article  Google Scholar 

  • Stapleton JA, Lavine M, Wolpert R, Nicolelis MAL, Simon SA (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26:4126–4138

    Article  CAS  Google Scholar 

  • Stapleton JA, Lavine M, Nicolelis MAL, Simon SA (2007) Ensembles of gustatory cortical neurons anticipate and discriminate between tastants in a single lick. Front Neurosci 1:161–174

    Article  Google Scholar 

  • Treesukosol Y, Lyall V, Heck GL, DeSimone JA, Spector AC (2007) A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice. Am J Physiol Regul Integr Comp Physiol 292:R1799–R1809

    CAS  Google Scholar 

  • Wang Y, Erickson RP, Simon SA (1993) Selectivity of lingual nerve fibers to chemical stimuli. J Gen Physiol 101:843–866

    Article  CAS  Google Scholar 

  • Wang Y, Erickson RE, Simon SA (1995) Modulation of chorda tympani nerve activity by lingual nerve stimulation. J Neurophysiol 73:1468–1483

    CAS  Google Scholar 

  • Yamamoto Y, Yuyama N, Kato T, Kawamura Y (1984) Gustatory responses of cortical neurons in the rats. l. Response characteristics. J Neurophysiol 51:616–635

    CAS  Google Scholar 

  • Yamamoto T, Yuyama N, Kato K, Kawamura Y (1988) Gustatory responses of cortical neurons in rats. II. information processing of taste quality. J Neurophysiol 53:1356–1369

    Google Scholar 

  • Yamamoto T, Yuyama N, Kato T, Kawamura Y (1989) Gustatory responses of cortical neurons in rats. III. Neural and behavioral measures compared. J Neurophysiol 53:1370–1386

    Google Scholar 

  • Yaxley S, Rolls ET, Sienkiewicz (1988) The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol & Behav 42:223–229

    Article  CAS  Google Scholar 

Download references

Acknowledgment

We thank Professor Alan Spector for clarifying some points regarding the ingestion of NaCl. This study was supported in part by NIH grant DC-01065 and grants from Philip Morris USA and Philip Morris International.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Duke University, Durham, NC, 27710, USA

    S. A. Simon, J. R. Stapleton & M. A. L. Nicolelis

  2. Department of Anesthesiology, Duke University, Durham, NC, 27710, USA

    S. A. Simon

  3. Center of Neuroengineering, Duke University, Durham, NC, 27710, USA

    S. A. Simon & M. A. L. Nicolelis

  4. Psychology and Neuroscience, Duke University, Durham, NC, 27710, USA

    M. A. L. Nicolelis

  5. Biomedical Engineering, Duke University, Durham, NC, 27710, USA

    M. A. L. Nicolelis

  6. J.B. Pierce Laboratory, 290 Congress Avenue, New Haven, CT, 06519, USA

    I. E. de Araujo

  7. Edmond and Lily Safra International Institute of Neuroscience of Natal, Natal, RN, Brazil, 59066-060

    M. A. L. Nicolelis

Authors
  1. S. A. Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. E. de Araujo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. R. Stapleton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. L. Nicolelis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. A. Simon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simon, S.A., de Araujo, I.E., Stapleton, J.R. et al. Multisensory Processing of Gustatory Stimuli. Chem. Percept. 1, 95–102 (2008). https://doi.org/10.1007/s12078-008-9014-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12078-008-9014-4

Keywords

Search

Navigation