ISSN: 1230-2813
Advances in Psychiatry and Neurology/Postępy Psychiatrii i Neurologii
Bieżący numer Archiwum Artykuły zaakceptowane O czasopiśmie Rada naukowa Bazy indeksacyjne Prenumerata Kontakt Zasady publikacji prac
SCImago Journal & Country Rank
1/2019
vol. 28
 
Poleć ten artykuł:
Udostępnij:
więcej
 
 
Artykuł przeglądowy

Sensory interaction theory: revision of the craniofacial region

Silvia Regina Dowgan Tesseroli de Siqueira
,
Manoel Jacobsen Teixeira

Data publikacji online: 2019/03/30
Plik artykułu:
Pobierz cytowanie
ENW
EndNote
BIB
JabRef, Mendeley
RIS
Papers, Reference Manager, RefWorks, Zotero
AMA
APA
Chicago
Harvard
MLA
Vancouver
 
 

INTRODUCTION

The investigation of sensory perception has been a field of scientific interest since the end of the 19th century. Although there are separated sensory modalities, there is also an integrated sensory system that is at least a part of the background of conscious perception, which began to be scientifically demonstrated in the second half of the 20th century. The Gate Control Theory of Melzack and Wall (1965) [1] provided clear evidence that different somatosensory stimuli (mediated by nerve fibres of small or large diameter) interact. The main observation was the suppression of pain sensation by tactile and other non-painful inputs. Melzack expanded this theory in 1999 [2] with the concept of the neuromatrix, a complex neural network. This concept posited a more complex neural interaction in the central nervous system which involved somatosensory, limbic and thalamocortical components, dependent on a time-space stimuli relation. Beyond the interaction of somatosensory inputs, Melzack argued, there is integration with special sensory modalities which have a role in the neural processing of perception [2].
Evidence-based studies of this interaction began to be published, especially on the orofacial area, and found that simple perception at the oral cavity integrates somatosensory, gustative and olfactory inputs. Gustative complaints have been reported by patients with trigeminal pain [3-7], and taste studies have shown the association between taste and smell [8, 9]. The temperature of chemical substances seems to impact olfactory and gustative thresholds [10-14], and there is an integration of somatosensory and special sensory modalities in the craniofacial region [15-17]. This review states a unified theory for craniofacial sensory interaction, which plays an important role in the vital functions of the conscious perception of the environment.

The dynamic process of sensory perception in the craniofacial area

The trigeminal system is the largest and most complex somatosensory system in the human body. There is an intense convergence in it of inputs from the oral and nasal mucosa, cornea, facial skin, lips, teeth, nose, dura mater, tongue, deep tissues and part of the auditory canal, which are processed in the central nervous system along with adjacent somatosensory inputs mediated by other cranial nerves (VII, IX, X) [18-21]. Its complexity is closely related to the evolutionary importance of this body area in survival and interaction with the environment and other beings [22]. Its functions include breathing, chewing, talking and swallowing, which depend on exteroceptive (e.g. vision, odours, oral sensations that coordinate chewing and swallowing with breathing) and interoceptive sensory inputs (e.g. levels of glucose, O2, CO2 in the blood flow) [18, 21].
Conscious and non-conscious efferent responses, such as salivation, muscular activity facial mimic, mastication and even hand movements to lead the food to the mouth [23], depend on the sensory system. This last one may be the reason for the proximity of the inferior third of the face and the hand in cortical representation of each side, and these responses might be impaired when the sensory system presents dysfunctions [24]. Moreover, not only does saliva depend on sensory interaction, it also facilitates sensory perception in the mouth [25, 26]. Taste is a complex interaction between gustative thresholds and temperature, odorants and texture of the food [17]; thus, any abnormality in this system could affect perception as a whole [16, 24, 27].
It is important to highlight the dynamic influence that sensory perception may present in the contexts of the internal or external environments. High levels of glycated haemoglobin have been associated with facial hypoalgesia in patients with diabetes mellitus [28], and there is an influence of the circadian cycle on sensory perception, depending on hormones and mediators [29, 30].
Women have lower sensory thresholds than men [31] due to hormonal modulation by oestrogen and progesterone [32, 33], neural mechanisms [34, 35] and psychosocial aspects [36, 37]. The genetic influence of the X chromosome is not well-defined and future studies are necessary, including in children before the sex maturation. On the other hand, ageing is related to a decrease of sensory perception [31, 38-41]; possible mechanisms include the decline of immune responses and regulation of neurogenesis [42], the use of medication, chronic processes, variation in the density and distribution of receptors and ionic channels and the composition of saliva and nasal mucus [43].
Cortical maps of sensory representation are dynamic and can change not only with time but also during an activity [44]. The receptive fields seem to be formed according to the simultaneous activation of the ascendant paths amplified in central areas by the circuitries of retransmission or the inhibitory neurons associated with them [45]. Thus, associated with the convergence of information there is a paradoxically divergent pattern [46, 47]. The descendent modulatory circuits permit the passage of some inputs to the detriment to others, and these are the pathophysiological mechanisms that underlie conscious sensory perception [48, 49]. It is also possible to observe the inhibition of pain sensations by the stimulation of periaqueductal grey substance or motor cortical areas [50].

Clinical and experimental evidence of sensory interaction

In recent decades, quantitative sensory testing protocols had been developed to elucidate the mechanisms involved in orofacial pain conditions [51-54]. Sensory abnormalities appear most often after trauma or in neuropathic conditions [6, 7, 24, 55-61]. The association between trigeminal abnormalities and altered taste perception has been shown [4, 62, 63], and supports orofacial sensory interaction. It is known that an increase in temperature may help in the detection of taste [64].
The unilateral stimulation of the tongue with sodium chlorate in patients with an injury in the contralateral chorda timpani nerve generated bilateral nuclear activation at the brainstem [65]. Gustative impairment after trigeminal surgery indicates the existence of central and peripheral sensorial interaction, as supported by animal studies [21, 66]. Injury to the lingual nerve, which has both trigeminal nerve and facial nerve fibres, leads to the faster regeneration of large fibres to the detriment of the smaller ones (pain, temperature and gustation), and corresponds to the symptoms of pain and dysgeusia in patients [67]. On the other hand, it has also been observed that olfactory threshold decrease impairs the trigeminal function at the nasal mucosa [15].
Despite the clear association of abnormal sensitivity with neuropathy, other orofacial conditions that are not neuropathic also present sensorial changes due to secondary hyperalgesia and central sensitization [18]; for example, temporomandibular disorders that have musculoskeletal mechanisms causing hyperalgesia and sensitization [68, 69]. Research on patients with persistent idiopathic facial pain has generated controversial results [6, 70, 71], and the possible explanations are a diagnosis of exclusion and that there are methodological differences in patients’ recruitment for the studies. This suggested that, according to the aetiology of the pain, the sensory loss pattern is variable. It is also important to consider that there are many drugs that are used for chronic pain control and that alter sensory thresholds, for example carbamazepine, often taken by the patients during the studies [63, 72].
The generalized pain of fibromyalgia is associated with several sensorial abnormalities, including taste and smell disorders [73], and facial palsy primarily involving the VII nerve is associated with secondary somatosensory differences in the trigeminal area [74]. Although the interaction between somatosensory, gustative and olfactory inputs has been widely accepted, and despite the hypothesis of chemosensory (gustation and olfaction) interaction with vision [47], only recently has it been demonstrated, in several studies, that there is interaction among somatosensation, gustation, olfaction, audition and vision [16, 75, 76]. Patients with trigeminal neuralgia who underwent a compression of the trigeminal ganglion as treatment experienced auditory and vision complaints [59], and odours can help in the determination of the location of a sound [77].

The special modalities: vision, audition, gustation and olfaction

The chemical senses, represented by gustation and olfaction, are highly integrated and comprise the taste sensation along with somatosensory information from the oral and nasal mucosa mediated by the trigeminal nerve [8, 9]. Different chemical neurons are specific for different chemical substances, but a single neuron can recognize a wide range of chemicals due to multiple signalling cascades [78, 79]. Chemical transduction depends on the recognition of the molecular structure according to the dilution of the component in saliva or nasal mucus [9, 79, 80].
Anosmia and hyposmia are common in the general population [15, 81] and can be associated with various conditions such as tumours, infections, nephropathies, epilepsy and neurodegenerative diseases [79, 82]. Women have lower olfactory thresholds and these abnormalities increase with ageing [81, 83]. Both anosmia and hyposmia have also been associated with neurodegenerative diseases (Parkinson’s, Alzheimer’s disease) as predictors [81, 84].
Ageusia and hypogeusia, characterized by loss of taste sensation, can be associated with several pain conditions at the oral cavity [4, 7, 8, 78, 85]. The electrical activity of gustation is processed at the geniculate (VII), petrosus (IX) and/or nodosus (X) ganglions and the gustative area of the solitary tract at the brainstem [86-88]. Factors such as appetite, blood concentrations of glucose and insulin may interfere in gustative perception [89, 90]. The need for the distribution of substances at the oral cavity in order to favour the detection of taste may be a clue as to the implications of trigeminal inputs for taste detection [79].

Craniofacial sensory interaction

Sensory receptors are connected to a highly flexible circuitry, capable of discriminating between several types of continuously flowing information from the environment. They generate precise responses determined by anatomic circuits that are potentiated according to the exposition to sensory stimuli, stored as memories [91, 92]. Consistency of perception depends on sensory integration according to the size of receptive fields of neurons, the correct inhibition of undesired stimuli and the convergence of data on cortical areas of association, which are more functional than topographic [21, 46, 93]. To understand craniofacial perception, it is essential to comprehend its multisensorial functions [94]. A large proportion of gustative and olfactory sensations are perceived during mastication [8, 95], and somatosensory participation helps in the determination of the location of taste at the tongue, even if there are olfactory inputs associated [96]. Taste has a somatosensory component itself that includes the texture and temperature of food, and spicy (pain and heat), menthol (cold) and carbonated (small pain fibres) sensations [12, 21, 78]. Saliva has an important role and its absence and reduction can interfere in oral sensations [25]. Its quality is also important and an imbalance in its components – such as peptides, glycoprotein, lipids, enzymes and histamine – can alter taste detection [97].
Several animal studies have elucidated the mechanisms involved in craniofacial sensorial interaction. The neurectomy of chorda timpani causes an increase of salty thresholds in rodents [98] and the neurectomy of the glossopharyngeal nerve increases the bitter taste threshold [99-102]. When the neurectomy of both is performed simultaneously, even if one of them regenerates, there is no normalization of these sensations, showing the interdependence between them for gustation [103]. After the neurectomy of chorda timpani, trigeminal and glossopharyngeal nerves, the level of sensory loss is higher when the lesion is closer to the peripheral tissues [104]. In the last decade it has been demonstrated that the subnucleous oralis of the trigeminal complex can also mediate gustative inputs [105]. The perception of taste is a mixture the activity of excitatory (glutamatergic) and inhibitory (gabaergic A) synapses at the brainstem and thalamus involving the trigeminal, facial, glossopharyngeal and vagus afferences [106]. Actually, a large part of gustative processing occurs at the brainstem due to the convergence of inputs conducted by the chorda timpani and glossopharyngeal afferents [107]. In frogs, depending on the chemical gustative stimuli at the tongue, there is an increase or reduction of antidromic activity, though the alteration of membrane potential with electrical stimuli cannot show these findings. This evidence supports peripheral mechanisms in the interaction between gustative and somatosensory afferences [108].
The rostral nucleus of the solitary tract is the first centre of gustative processing and modulation, followed by the parabrachial nucleus. There is evidence for the involvement of delta-opioid receptors in this process [109]. The circuitry of gustative sensation at the tongue involves known gustative areas (the central rostral nucleus of the solitary tract, synapses with geniculate axons, projections to the parabrachial nucleus at the pons), but also the lateral part of the rostral nucleus of the solitary tract, which also receives trigeminal afferents [110], and the ventral area of the solitary tract and reticular formation, responsible for the interaction with oral motor reflexes, and important for mastication and swallowing [21, 111-113]. The evidence indicates that there is also visceral modulation and the influence of previous gustative experiences by descendent pathways from the anterior cortex. The electrical stimulation of the central nucleus of the amygdala modulates the intensity of the type of gustative input that is transmitted by the parabrachial nucleus [114]. Following gustative stimulation by a sweet substance there is activation of chemoreceptors at the nasal epithelium mediated by trigeminal paths [115]. It is evident that neurons from the solitary tract not only protrude but also receive axons from the parabrachial nucleus and that both communicate to the contralateral side [116].
The parabrachial nucleus connects to the gustative cortex via the parvicellular part of the ventroposteromedial nucleus of the thalamus, which sends back inhibitory projections that modulate gustative sensations [117]. Axons from the hippocampus project not only to the thalamus and hypothalamus but also to the limbic system and to the visual, auditory, somatosensory, olfactory and gustative cortexes. They may be responsible for long-term potentiation (LTP) resulting in the sensory abnormalities observed in clinical studies [118].
During eating, each sensory neuron is apparently specific to each stimulus; however, in the central nervous system the groups of neurons from analogous sensations determine its magnitude, which becomes complex due to the convergence of different modalities on these centres. Animal studies have shown that any taste mixtures lead to ambiguous responses [119], and that the highly concentrated taste modality is the only one that is usually clearly identified in these mixtures. Some neurons even respond better to the mixture than to the taste modality isolated because they are bombarded with action potentials and thus can amplify the highly concentrated taste in that mixture [120]. It is known that sweet and bitter tastes use segregated circuitries in the CNS but have peripheral modulation. Even with this segregated circuitry, the projections of each taste modality reach areas of association that are completely superposed for salty, sour, bitter and sweet [9, 121].
The pattern of cortical activation depends on the emotional characteristic of the taste modality (pleasant or unpleasant), even in flavours designed to activate cortical areas [121]. The model mostly used as an example for the gustative interaction is the inhibition of the sweet taste when bitter is present. This happens because the cationic channel TRPM5, involved in the transmission of sweetness, is inhibited by some bitter substances as such quinine due to an acceleration of channel closing [122]. This modulation is completely peripheral. The taste buds are not uniformly distributed, but depend on the nerve (X, IX or VII), which also can impair the perception of flavour [123]. Central analgesia by breastfeeding is mediated by the activation by sugars of the gustative paths that activate pain-suppressing areas such as the periaqueductal grey substance and the nucleus raphe magnus [124].
A simple injury to the trigeminal fibres has been shown in animal studies to alter taste detection and supports the need of trigeminal integrity for gustative sensitivity [125].
The trigeminal system is also closely connected with the olfactory system [15, 126], and peripheral adaptive mechanisms seem to reduce trigeminal responsiveness in anosmia and hyposmia [15]. This interaction occurs in the direct activation of the trigeminal fibres at the nasal mucosa by the same odorants [127].

CONCLUSIONS

The trigeminal system seems to mediate olfactory and gustative sensations in cortical associative centres, which implicates somatosensory inputs in the determination of the location of the stimulus, besides other characteristics. This role may be weakened in the occurrence of chronic conditions such as craniofacial pain, resulting in a sensorial imbalance, and dysfunction of orofacial perception. Despite the wide range of evidence so far accumulated, there is a lack of studies investigating the integration between vision and audition with the chemosenses (gustation and olfaction) and somatosensory inputs, which are promising lines of research for the future. Animal models for the investigation of cortical maps of isolated and associated sensorial modalities in healthy or pathological conditions will clarify the still-obscure mechanisms that underlie these observations.

Conflict of interest

Absent.

Financial support

Absent.

References

1. Melzack R, Wall PD. Pain mechanisms: a new theory. Science 1965; 150: 971-979.
2. Melzack R. From the gate to the neuromatrix. Pain 1999 (Suppl 6): S121-S126.
3. Grushka M, Epstein JB, Gorsky M. Burning mouth syndrome and other oral sensory disorders: a unifying hypothesis. Pain Res Manag 2003; 8: 133-135.
4. Jääskeläinen SK, Woda A. Burning mouth syndrome. Cephalalgia 2017; 37: 627-647.
5. Siqueira SR, Nóbrega JCM, Teixeira MJ, Siqueira JTT. Olfactory threshold increase in trigeminal neuralgia after balloon compression. Clin Neurol Neurosurg 2006; 108: 721-725.
6. Siqueira SR, Teixeira MJ, de Siqueira JT. Somatosensory investigation of patients with orofacial pain compared with controls. J Neuropsychiatry Clin Neurosci 2014; 26: 376-381.
7. Siviero M, Teixeira MJ, Siqueira JTT, Siqueira SRDT. Somesthetic, gustatory, olfactory function and salivary flow in patients with trigeminal neuropathic pain. Oral Dis 2010; 16: 482-487.
8. Bartoshuk LM. Clinical psychophysics of taste. Gerodontics 1988; 4: 249-255.
9. Iannilli E, Gudziol V. Gustatory pathway in humans: A review of models of taste perception and their potential lateralization. J Neurosci Res 2019; 97: 230-240.
10. Breza JM, Curtis KS, Contreras RJ. Temperature modulates taste responsiveness and stimulates gustatory neurons in the rat geniculate ganglion. J Neurophysiol 2006; 95: 674-685.
11. Cruz A, Green BG. Thermal stimulation of taste. Nature 2000; 403: 889-892.
12. Lemon CH. Modulation of taste processing by temperature. Am J Physiol Regul Integr Comp Physiol 2017; 313: R305-R321.
13. Schiffman SS, Sattely-Miller EA, Graham BG, Bennett JL, Booth BJ, Desai N, Bishay I. Effect of temperature, pH, and ions on sweet taste. Physiol Behav 2000; 68: 469-481.
14. Stone H. Influence of temperature on olfactory sensitivity. J Appl Physiol 1963; 18: 746-751.
15. Frasnelli J, Hummel T. Interactions between the chemical senses: trigeminal function in patients with olfactory loss. Int J Psychophysiol 2007; 65: 177-181.
16. Sperdin HF, Cappe C, Murray MM. Auditory-somatosensory multisensory interactions in humans: dissociating detection and spatial discrimination. Neuropsychol 2010; 48: 3696-705.
17. Wilson DM, Lemon CH. Modulation of central gustatory coding by temperature. J Neurophysiol 2013; 110: 1117-1129.
18. Sessle BJ. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000; 11: 57-91.
19. Talbot JD, Marrett S, Evans AC, Meyer E, Buchnell MC, Duncan GH. Multiple representations of pain in human cerebral cortex. Science 1991; 251: 1355-1358.
20. Toda T, Taoka M. Converging patterns of inputs from oral structures in the postcentral somatosensory cortex of conscious macaque monkeys. Exp Brain Res 2004; 158: 43-49.
21. Van der Cruyssen F, Politis C. Neurophysiological aspects of the trigeminal sensory system: an update. Rev Neurosci 2018; 29: 115-123.
22. Murakami Y, Kuratani S. Brain segmentation and trigeminal projections in the lamprey; with reference to vertebrate brain evolution. Brain Res Bull 2008; 75: 218-224.
23. Lund JP, Kolta A. Generation of the central masticatory pattern and its modification by sensory feedback. Dysphagia 2006; 21: 167-174.
24. Ichida MC, de Almeida AN, da Nobrega JC, Teixeira MJ, de Siqueira JT, de Siqueira SR. Sensory abnormalities and masticatory function after microvascular decompression or balloon compression for trigeminal neuralgia compared with carbamazepine and healthy controls. J Neurosurg 2015; 122: 1315-1323.
25. Canon F, Neiers F, Guichard E. Saliva and Flavor Perception: Perspectives. J Agric Food Chem 2018; 66: 7873-7879.
26. Nagler RM, Hershkovich O. Sialochemical and gustatory analysis in patients with oral sensory complaints. J Pain 2004; 5: 56-63.
27. Hospedales T, Vijayakumar S. Multisensory oddity detection as bayesian inference. PLoS One 2009; 4: e4205.
28. Arap A, Siqueira SRDT, Silva CB, Teixeira MJ, Siqueira JTT. Trigeminal pain and quantitative sensory testing in painful peripheral diabetic neuropathy. Arch Oral Biol 2010; 55: 486-493.
29. Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A. Organization of circadian functions: interaction with the body. Prog Brain Res 2006; 153: 341-360.
30. Segal JP, Tresidder KA, Bhatt C, Gilron I, Ghasemlou N. Circadian control of pain and neuroinflammation. J Neurosci Res 2018; 96: 1002-1020.
31. Silva LA, Lin SM, Teixeira MJ, Siqueira JTT, Jacob-Filho W, Siqueira SR. Sensorial differences according to sex and ages. Oral Dis 2014; 20: e103-e110.
32. Alves B, Ibuki F, Gonçalves AS, Teixeira MJ, De Siqueira SRDT. Influence of Sexual Hormones on Neural Orofacial Perception. Pain Med 2017; 18: 1549-1556.
33. Bereiter DA, Cioffi JL, Bereiter DF. Oestrogen receptor-immunoreactive neurons in the trigeminal sensory system of male and cycling female rats. Arch Oral Biol 2005; 50: 971-979.
34. Bereiter DA, Shen S, Benetti AP. Sex differences in amino acid release from rostral trigeminal subnucleus caudalis after acute injury to the TMJ region. Pain 2002; 98: 89-99.
35. Cairns BE, Hu JW, Arendt-Nielsen L, Sessle BJ, Svensson P. Sex-related differences in human pain and rat afferent discharge evoked by injection of glutamate into the masseter muscle. J Neurophysiol 2001; 86: 782-791.
36. Fillingim RB, King CD, Silva MCR, et al. Sex, Gender, and Pain: A Review of Recent Clinical and Experimental Findings. J Pain 2009; 10: 447-485.
37. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, et al. The Consensus Working Group of the Sex, Gender, and Pain SIG of the IASP Studying sex and gender differences in pain and analgesia: A consensus report. Pain 2007; 132: S26-S45.
38. Heckmann JG, Lang CJ. Neurological causes of taste disorders. Adv Otorhinolaryngol 2006; 63: 255-264.
39. Heft MW, Robinson ME. Age differences in orofacial sensory thresholds. J Dent Res 2010; 89: 1102-1105.
40. Nordin S, Razani LJ, Markison S, et al. Age-Associated Increases in Intensity Discrimination for Taste. Exp Aging Res 2003; 29: 371-381.
41. Petersen P, Gao C, Rossel P, Qvist P, Arendt-Nielsen L, Gregersen H, Rewes AM. Sensory and biomechanical responses to distension of the normal human rectum and sigmoid colon. Digestion 2001; 64: 191-199.
42. Rawson NE, LaMantia AS. A speculative essay on retinoic acid regulation of neural stem cells in the developing and aging olfactory system. Exp Gerontol 2007; 42: 46-53.
43. Rawson NE. Olfactory Loss in Aging. Sci Aging Knowl Environ 2006; 5: 6-14.
44. Mountcastle VB. The columnar organization of the neocortex. Brain 1997; 120: 702-722.
45. Gardner EP, Hërnäläinen HA, Palmer CI, Warren S. Touching the outside world: representation of motion and direction within primary somatosensory cortex. In: Lund JS (ed.). Sensory processing in mammalian brain: neural substrates and experimental strategies. New York: Oxford Univ Press; 1989, p. 49-66.
46. Gardner EP, Kandel ER. Tato. In: Kandel ER, Schwartz JH, Jessell TM (eds.). Princípios da Neurociência. 4th ed. Rio de Janeiro: Manole; 2003, p. 451-471.
47. Liberati D, Bedarida L, Brandazza P, Cerutti S. A model for the cortico-cortical neural interaction in multisensory-evoked potentials. IEEE Trans Biomed Eng 1991; 38: 879-890.
48. Bennett MR. Development of the concept of mind. Aust N Z J Psychiatr 2007; 41: 943-956.
49. Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, et al. Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 2008; 7: 1013-1020.
50. Basbaum AI, Jessell TM. Pain perception. In: Kandel ER, Schwartz JH, Jessell TM. Principles of Neuroscience. 4th ed. Rio de Janeiro: Manole; 2003, p. 473-491.
51. Eliav E, Gracely RH, Nahlieli O, Benoliel R. Quantitative sensory testing in trigeminal nerve damage assessment. J Orofac Pain 2004; 18: 339-344.
52. Jääskeläinen SK. Clinical neurophysiology and quantitative sensory testing in the investigation of orofacial pain and sensory function. J Orofac Pain 2004; 18: 85-107.
53. Pigg M, Baad-Hansen L, Svensson P, Drangsholt M, List T. Reliability of intraoral quantitative sensory testing (QST). Pain 2009; 148: 220-226.
54. Zhou P, Chen Y, Zhang J, Wang K, Svensson P. Quantitative sensory testing for assessment of somatosensory function in human oral mucosa: a review. Acta Odontol Scand 2018; 76: 13-20.
55. Grushka M, Ching V, Epstein J. Burning mouth syndrome. Adv Otorhinolaryngol 2006; 63: 278-287.
56. Nasri C, Teixeira MJ, Okada M, Formigoni G, Heir G, Siqueira JT. Burning mouth complaints: clinical characteristics of a Brazilian sample. Clinics 2007; 62: 561-566.
57. Petersen KL, Rowbotham MC. Natural history of sensory function after herpes zoster. Pain 2010; 150: 83-92.
58. Sardella A, Demarosi F, Barbieri C, Lodi G. An up-to-date view on persistent idiopathic facial pain. Minerva Stomatol 2009; 58: 289-299.
59. Siqueira SR, da Nóbrega JC, de Siqueira JT, Teixeira MJ. Frequency of postoperative complications after balloon compression for idiopathic trigeminal neuralgia: prospective study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006; 102: e39-e45.
60. Siqueira SRDT, Lara C, Nóbrega JCM, Siqueira JTT, Teixeira MJ. Sensitive evaluation of patients with idiopathic trigeminal neuralgia treated with functional neurosurgery. Pain Clin 2006; 18: 87-92.
61. Siviero M, Alvarez FK, Okada M, Teixeira MJ, Siqueira JTT, Siqueira SRDT. Facial sensibility of patients with trigeminal neuralgias. Clin Neurol Neurosurg 2011; 113: 268-271.
62. Siviero M, Teixeira MJ, Siqueira JTT, Siqueira SRDT. Rapid communication: Central Mechanisms in burning mouth syndrome involving the olfactory nerve: preliminary study. Clinics 2011; 66: 509-512.
63. Etoh S, Kawahira K, Ogata A, Shimodozono M, Tanaka N. Relationship between dysgeusia and dysesthesia in stroke patients. Int J Neurosci 2008; 118: 137-147.
64. Bajec MR, Pickering GJ. Thermal taste, PROP responsiveness, and perception of oral sensations. Physiol Behav 2008; 95: 581-590.
65. Onoda K, Kobayakawa T, Ikeda M, Saito S, Kida A. Laterality of human primary gustatory cortex studied by MEG. Chem Senses 2005; 30: 657-666.
66. Shiau CE, Lwigale PY, Das RM, Wilson SA, Bronner-Fraser M. Robo2-Slit1 dependent cell-cell interactions mediate assembly of the trigeminal ganglion. Nat Neurosci 2008; 11: 269-276.
67. Holland GR. Experimental trigeminal nerve injury. Crit Rev Oral Biol Med 1996; 7: 237-258.
68. Welte-Jzyk C, Pfau DB, Hartmann A, Daubländer M. Somatosensory profiles of patients with chronic myogenic temporomandibular disorders in relation to their painDETECT score. BMC Oral Health 2018; 18: 138.
69. Younger JW, Shen YF, Goddard G, Mackey SC. Chronic myofascial temporomandibular pain is associated with neural abnormalities in the trigeminal and limbic systems. Pain 2010; 149: 222-228.
70. Forssell H, Tenovuo O, Silvoniemi P, Jääskeläinen SK. Differences and similarities between atypical facial pain and trigeminal neuropathic pain. Neurology 2007; 69: 1451-1459.
71. Lang E, Kaltenhäuser M, Seidler S, Mattenklodt P, Neundörfer B. Persistent idiopathic facial pain exists independent of somatosensory input from the painful region: findings from quantitative sensory functions and somatotopy of the primary somatosensory cortex. Pain 2005; 118: 80-91.
72. Flor H, Rasche D, Islamian AP, Rolko C, Yilmaz P, Ruppolt M, et al. Subtle Sensory Abnormalities Detected by Quantitative Sensory Testing in Patients with Trigeminal Neuralgia. Pain Physician 2016; 19: 507-518.
73. Kosek E, Ekholm J, Hansson P. Sensory dysfunction in fibromyalgia patients with implications for pathogenic mechanisms. Pain 1996; 68: 375-383.
74. Kohjitani A, Miyawaki T, Kasuya K, Shimada M. Sympathetic activity-mediated neuropathic facial pain following simple tooth extraction: a case report. Cranio 2002; 20: 135-138.
75. Bicchi A, Scilingo EP, Ricciardi E, Pietrini P. Tactile flow explains haptic counterparts of common visual illusions. Brain Res Bull 2008; 75: 737-741.
76. Livermore A, Hummel T. The influence of training on chemosensory event-related potentials and interactions between the olfactory and trigeminal systems. Chem Senses 2004; 29: 41-51.
77. Niemi M, Laaksonen JP, Forssell H, Jääskeläinen S, Aaltonen O, Happonen RP. Acoustic and neurophysiologic observations related to lingual nerve impairment. Int J Oral Maxillofac Surg 2009; 38: 758-765.
78. Bartoshuk LM, Beauchamp GK. Chemical senses. Ann R Tev Psychol 1994; 45: 419-449.
79. Buck LB. Olfation and gustation: the chemical senses. In: Kandel ER, Schwartz JH, Jessell TM (eds.). Principles of Neuroscience. 4th ed. Rio de Janeiro: Manole; 2003, p. 625-647.
80. Shepherd GM. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 2007; 1121: 87-101.
81. Doty RL. The olfactory system and its disorders. Semin Neurol 2009; 29: 74-81.
82. Sullivan SL, Ressler KJ, Buck LB. Spatial patterning and information coding in the olfactory system. Curr Opin Genet Dev 1995; 5: 516-523.
83. Silva LAD, Jaluul O, Teixeira MJ, Siqueira JTT, Jacob Filho W, Siqueira SRDT. Quantitative sensory testing in elderly: longitudinal study. Arq Neuropsiquiatr 2018; 76: 743-750.
84. Bromley SM, Doty RL. Olfaction in dentistry. Oral Dis 2010; 16: 221-232.
85. Grushka M, Sessle B. Taste dysfunction in burning mouth syndrome. Gerodontics 1988; 4: 256-258.
86. Bradley RM, Grabauskas G. Neural circuits for taste. Excitation, inhibition, and synaptic plasticity in the rostral gustatory zone of the nucleus of the solitary tract. Ann N Y Acad Sci 1998; 855: 467-474.
87. Shikama Y, Kato T, Nagaoka U, Hosoya T, Katagiri T, Yamaguchi K, Sasaki H. Localization of the gustatory pathway in the human midbrain. Neurosci Lett 1996; 218: 198-200.
88. Smith DV, Li CS, Davis BJ. Excitatory and inhibitory modulation of taste responses in the hamster brainstem. Ann N Y Acad Sci 1998; 855: 450-456.
89. Reilly S. The role of the gustatory thalamus in taste-guided behavior. Neurosci Biobehav Rev 1998; 22: 883-901.
90. Small DM. Central gustatory processing in humans. Adv Otorhinolaryngol 2006; 63: 191-220.
91. Gardner EP, Palmer CI. Simulation of motion on the skin. I. Receptive fields and temporal frequency coding by cutaneous mechanoreceptors of OPTACON pulses delivered to the hand. J Neurophysiol 1989; 62: 1410-1436.
92. Kandel ER. O sistema nervoso e o comportamento. In: Kandel ER, Schwartz JH, Jessell TM (eds.). Princípios da Neurociência. 4th ed. Rio de Janeiro: Manole; 2003, p. 5-18.
93. Favorov O, Kelly DG. Miunicolumnar organization within somatosensory cortical segregates. II. Emergent functional properties. Cereb Cortex 1994; 4: 428-442.
94. Sherrington C. The integrative action of the nervous system. 2nd ed. New Haven: Yale Univ. Press; 1947.
95. Cerf-Ducastel B, Murphy C. fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses 2001; 26: 625-637.
96. Savage CW. The measurement of sensation: a critique of perceptual psychophysics. Univ. Berkeley: California Press; 1970.
97. Song Q, Lange T, Spahr A, Adler G, Bode GJ. Characteristic distribution pattern of Helicobacter pylori in dental plaque and saliva detected with nested PCR. J Med Microbiol 2000; 49: 349-353.
98. Kopka SL, Geran LC, Spector AC. Functional status of the regenerated chorda tympani nerve as assessed in a salt taste discrimination task. Am J Physiol Regul Integr Comp Physiol 2000; 278: R720-R731.
99. Travers JB, Grill HJ, Norgren R. The effects of glossopharyngeal and chorda tympani nerve cuts on the ingestion and rejection of sapid stimuli: and electromyographic analysis in the rat. Behav Brain Res 1987; 25: 233-246.
100. Grill HJ, Schwartz GJ, Traves J. The contribution of gustatory nerve input to oral motor behavior and fluid intake-based preference: I. Effects of chorda tympani or glossopharyngeal nerve section in the rat. Brain Res 1991; 573: 95-104.
101. King CT, Garcea M, Spector AC. Glossopharyngeal nerve regeneration is essential for the complete recovery of quinine-stimulated oromotor rejection behaviors and central patterns of neuronal activity in the nucleus of the solitary tract in the rat. J Neurosci 2000; 20: 8426-8434.
102. King CT, Travers SP, Rowland NE, Garcea M, Spector AC. Glossopharyngeal nerve transaction eliminates quinine-stimulated fos-like immunoreactivity in the nucleus of the solitary tract: implications for a functional topography of gustatory nerve input in rats. J Neurosci 1999; 19: 3107-3121.
103. Spector AC. The functional consequences of gustatory nerve regeneration as assessed behaviorally in a rat model. Chemical Senses 2005; 30: i66-i67.
104. Hendricks SJ, Sollars SI, Hill DL. Injury-induced functional plasticity in the peripheral gustatory system. J Neurosci 2002; 22: 8607-8613.
105. Dallel R, Ricard O, Raboisson P. Organization of parabrachial projections from the spinal trigeminal nucleus oralis: an anterograde tracing study in the rat. J Comp Neurol 2004; 470: 181-191.
106. Bradley RM, King MS, Wang L, Shu X. Neurotransmitter and neuromodulator activity in the gustatory zone of the nucleus tractus solitarius. Chem Senses 1996; 21: 377-385.
107. Grabauskas G, Bradley RM. Synaptic interactions due to convergent input from gustatory afferent fibers in the rostral nucleus of the solitary tract. J Neurophysiol 1996; 76: 2919-2927.
108. Kutynal FA, Bernard R. Effects of antidromic activity in gustatory nerve fibers on taste disc cells of the frog tongue. J Comparative Physiol 1977; 118: 291-306.
109. Zhu M, Cho YK, Li CS. Activation of delta-opioid receptors reduces excitory input to putative gustatory cells within the nucleus of the solitary tract. J Neurophysiol 2009; 101: 258-268.
110. Krout KE, Loewy AD. Parabrachial nucleus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 2000; 428: 475-494.
111. Monroe S, Di Lorenzo PM. Taste responses in neurons in the nucleus of the solitary tract that do and do not project to the parabrachial pons. J Neurophysiol 1995; 74: 249-257.
112. Travers SP, Hu H. Extranuclear projections of rNST neurons expressing gustatory-elicited Fos. J Comp Neurol 2000; 427: 124-138.
113. Zaidi FN, Todd K, Enquist L, Whitehead MC. Types of taste circuits synaptically linked to a few geniculate ganglion neurons. J Comp Neurol 2008; 511: 753-772.
114. Lundy RF Jr, Norgren R. Pontine gustatory activity is altered by electrical stimulation in the central nucleus of the amygdala. J Neurophysiol 2001; 85: 770-783.
115. Ohmoto M, Matsumoto I, Yasuoka A, Yoshihara Y, Abe K. Genetic tracing of the gustatory and trigeminal neural pathways originating from T1R3-expressing taste receptor cells and solitary chemoreceptor cells. Mol Cell Neurosci 2008; 38: 505-517.
116. Cho YK, Li CS. Gustatory neural circuitry in the hamster brain stem. J Neurophysiol 2008; 100: 1007-1019.
117. Mao L, Cho YK, Li CS. Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus. Am J Physiol Regul Integr Comp Physiol 2008; 294: R1461-R1473.
118. Cenquizca LA, Swanson LW. Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 2007; 56: 1-26.
119. Ganchrow D, Erickson RP. Taste quality and intensity: lessons from the Morrison technique. Physiol Behav 2000; 69: 121-133.
120. Chen JY, Di Lorenzo PM. Responses to binary taste mixtures in the nucleus of the solitary tract: neural coding with firing rate. J Neurophysiol 2008; 99: 2144-2157.
121. Accolla R, Bathellier B, Petersen CC, Carleton A. Differential spatial representation of taste modalities in the rat gustatory cortex. J Neurosci 2007; 27: 1396-1404.
122, Talavera K, Yasumatsu K, Yoshida R, Margolskee RF, Voets T, Ninomiya Y, Nilius B. The taste transduction channel TRPM5 is a locus for bitter-sweet taste interactions. FASEB J 2008; 22: 1343-1355.
123. Eram M, Michel WC. Heterogeneous distribution of taste cells in facial and vagal nerve-innervated taste buds. Neuroscience 2006; 138: 339-350.
124. Anseloni VC, Ren K, Dubner R, Ennis M. A brainstem substrate for analgesia elicited by intraoral sucrose. Neuroscience 2005; 133: 231-243.
125. Berridge KC, Fentress JC. Trigeminal-taste interaction in palatability processing. Science 1985; 228: 747-750.
126. Frasnelli J, Schuster B, Hummel T. Interactions between olfaction and the trigeminal system: what can be learned from olfactory loss. Cereb Cortex 2007; 17: 2268-2275.
127. Frasnelli J, Heilmann S, Hummel T. Responsiveness of human nasal mucosa to trigeminal stimuli depends on the site of stimulation. Neurosci Lett 2004; 362: 65-69.
This is an Open Access journal, all articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0). License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
POLECAMY
© 2019 Termedia Sp. z o.o. All rights reserved.
Developed by Bentus.
PayU - płatności internetowe