This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Rousseaux, M. Articles by Romon, M. Search for Related Content PubMed PubMed Citation Articles by Rousseaux, M. Articles by Romon, M.

(Stroke. 1996;27:2328-2330.)
© 1996 American Heart Association, Inc.

Articles

Disorders of Smell, Taste, and Food Intake in a Patient With a Dorsomedial Thalamic Infarct

M. Rousseaux, MD, PhD; P. Muller, MD; I. Gahide, MD; Y. Mottin, PhD M. Romon, MD

the Service de Reeducation et Convalescence Neurologiques (M. Rousseaux) and the Service de Nutrition (M. Romon), Centre Hospitalier Universitaire, Lille; and the Service de Neurologie (P.M., I.G.) and the Service d'Oto-Rhino-Laryngologie (I.G.), Centre Hospitalier Universitaire, Nice, France.

Correspondence to Dr M. Rousseaux, Service de Reeducation et Convalescence Neurologiques, Hopital Swynghedauw, Centre Hospitalier Universitaire, 59037 Lille Cedex, France.

	Abstract

Top Abstract Introduction Case Report Discussion References

 
Background We report that a lasting deficit in the hedonic character of olfactory and gustatory perception can be observed in bilateral dorsomedial and intralaminar thalamic lesions.

Case Description A 68-year-old patient abruptly presented with vigilance disorders associated with a reduction of olfactory and gustatory perceptions. A severe drop in appetite for foods and a weight loss of 10 kg were observed, which were partially reversed with time. Two years later, the main persisting disorder was a change in the quality of perceptions: odors and taste were perceived either in a neutral way, their pleasant character having disappeared, or as unpleasant. However, identification was preserved. MRI showed that lesions principally involved the dorsomedial thalamic nuclei and the adjacent part of the intralaminar nuclei.

Conclusions This case suggests that the dorsomedial thalamus may play a role in the hedonic perception of food, thus affecting short-term regulation of food intake, and may possibly have a role in the long-term control of body weight.

Key Words: appetite regulation • cerebral infarction • smell • taste • thalamus

	Introduction

Top Abstract Introduction Case Report Discussion References

 
The role of dorsomedial nuclei lesions has been suggested to explain disorders of odor recognition and identification in Korsakoff's syndrome,^{1 2} whereas Potter and Butters³ have described unilateral odor discrimination impairment in a patient presenting with a unilateral lesion of the dorsomedial nucleus.

The aim of this report is to describe the disappearance of the hedonic character of olfactory and gustatory perceptions that can be observed after bilateral dorsomedial thalamic nuclei injury; this disappearance can be associated with reduction of food intake and severe weight loss, suggesting a yet unrecognized role of the thalamus in food intake and body weight regulation.

	Case Report

Top Abstract Introduction Case Report Discussion References

 
A 68-year-old woman, whose weight had been stable at 65 kg for at least 10 years, abruptly presented in 1993 with horizontal diplopia that lasted for a few seconds and was followed by a loss of consciousness for about half an hour. Isolated disorientation persisted for a few hours. In the following days, she complained of marked alteration of olfactory and gustatory perceptions. She had an aversion to food, characterized by early interruption of food intake after the beginning of meals and a reduction in meal size. This resulted in a weight loss of 10 kg within a few months. Then, despite the persistence of impaired perception, her food intake improved. She gained 5 kg in 2 years, and her weight stabilized at 60 kg.

Two years later, the main objective disorder was a perceptual change: perceptions that used to be very pleasant before (perfume, flowers, milk products and cheese, fresh vegetables, dried sausages, desserts, and coffee) were no longer associated with an affective correlate, whereas some that were previously more neutral or less pleasant (washing powders, some vegetables, wine, not quite fresh meat, and fish) were perceived as unpleasant. On neurological examination, there was no motor, sensory, or oculomotor abnormality. The patient did not complain of memory or attention disorders. Results of a short neuropsychological assessment were within normal limits according to the Compendium of Neuropsychological Tests⁴ : Stroop Test, Trail-Making Test part B, Brown-Peterson paradigm, logical memory on the Wechsler Memory Scale–Revised, and Standard Progressive Matrices.

CT and MRI (3-mm-thick horizontal and coronal slices) showed an isolated and bilateral paramedian thalamic infarction (Fig 1). Three-dimensional reconstruction using the Schaltenbrand and Wahren atlas⁵ revealed that both infarcts extended in the substantia periventricularis, the anterior part of the nucleus dorsomedialis, and the adjacent lamella medialis (Fig 2). A cerebral blood flow study using hexamethylpropyleneamine oxime revealed mild bilateral thalamic hypofixation and normal activity in the frontal cortex.

View larger version (496K): [in this window] [in a new window]   Figure 1. T2 sequences on MRI (repetition time, 4000 seconds; echo time, 108 seconds).

View larger version (35K): [in this window] [in a new window]   Figure 2. Three-dimensional reconstruction of the lesion, using the Schaltenbrand and Wahren atlas, on the left (top) and right (bottom) thalamus. Lpo indicates lateropolaris nucleus; Apr, anteroprincipalis nucleus; M, dorsomedial nucleus; Lam, intralaminar nuclei; D, dorsolateral nuclei; Pu, pulvinar; Hb, habenula; Put, putamen; and Cd, caudate nucleus.

Olfactory and gustatory perceptions were more extensively evaluated. This patient did not smoke and had no history of diseases known to affect olfaction. Results of electrogustometry were normal. Fundamental tastes (salt, sweet, bitter, acid) were rapidly and accurately identified. Taste identification tests were performed by placing two series of 10 items on the tongue: foods and spices (salt, coffee, mustard, cinnamon, curry, licorice, sugar, pepper, vinegar, chocolate) and fruits and vegetables (lemon, banana, carrot, orange, strawberry, apple, endive, tomato, kiwi, avocado). The patient's responses were at the lower limit of the five controls for oral naming and within normal limits for forced choice recognition (1/4) (Table).

View this table: [in this window] [in a new window]   Table 1. Normal Performance in Tests of Identification and Memory of Odors and Flavors

With respect to smell, the patient reported no deficit of odor detection in her daily life and was able to accurately identify ether and denatured alcohol. A smell-recognition test was performed with the help of an odor sampling collection (Loto des Odeurs, Nathan). Two series of 10 stimuli were presented, each for 5 seconds: flowers (mimosa, pink, rose, lily, lilac, violet, orange flower, lily of the valley, mint, lavender) and fruits (melon, apple, grapefruit, banana, pear, strawberry, pineapple, lemon, apricot, mandarin). The patient's performance was normal in naming and forced-choice recognition (1/4) (Table). A test of olfactory memory was performed a few months later, using the same stimuli (presentation time, 5 seconds) to be recognized after a 30-second delay (forced choice, 1/3); no deficit was observed.

Before the stroke, the patient's eating habits, as reported in a questionnaire, consisted of three meals a day; she never ate snacks, had no nibbling behavior, and would start eating out of social habit without feeling hungry. After the stroke, this eating pattern remained the same. Furthermore, food choice remained the same. Whatever she ate, food was perceived as "tasteless" within 2 or 3 minutes. In the early period after the stroke, food intake was stopped very quickly, but this behavior progressively returned to normal.

	Discussion

Top Abstract Introduction Case Report Discussion References

 
Even though neuroradiological investigations were not performed shortly after the initial event, reported clinical symptoms such as vigilance disorders and diplopia are characteristic of unilateral or bilateral thalamic infarcts.^{6 7} Lesions selectively involved the middle part of dorsomedial nuclei on both sides and the adjacent intralaminar structures without any damage to the ventroposteromedial nuclei, which are the relay of somatosensory paths coming from the face and tongue and convey taste information onto the parietal cortex. More anterior thalamic and hypothalamic structures were also spared.

These anatomic structures are integrated in circuits that play a role in the analysis of olfactory and gustatory stimuli. In the monkey, cells belonging to the dorsomedial nucleus are activated (or more rarely inhibited) by stimulation of the olfactory bulb,⁸ and projections from the bulb are preferential for the medial magnocellular area.

Permanent deficits of odor identification have been described in unilateral⁹ and bilateral¹⁰ medial temporal lesions and also in lesions of the orbitofrontal cortex.^{3 9} Potter and Butters³ described a patient presenting with a unilateral tumoral lesion of the dorsomedial and intralaminar thalamic nuclei, which had an ipsilateral deficit in odor discrimination. In our case, the excellent preservation of odor and taste identification in the late phase might be explained by the preservation of the main pathway associating the olfactory bulb to the prepiriform cortex and further to the orbitofrontal cortex, which may have allowed a progressive recovery during 2 years.

The most permanent problem was a change of the perceptual quality of stimuli, which were perceived as neutral or unpleasant. Such a disorder has been described in a few cases for smell and possibly for taste in nasopharyngeal and olfactory bulb lesions¹¹ and in multiple sclerosis.¹² Most parosmias are associated with unpleasant perceptions during olfactory stimulations, a symptom that may also be observed during epileptic seizures of the uncus. This could be related to hyperactivity of corresponding temporal neurons due to deafferentiation or direct excitation.

In animals and humans, body weight is regulated by short- and long-term control factors.¹³ This case history illustrates the potential role of hedonic sensations in the control of food intake and in the short-term regulation of weight. Most studies of the neurophysiological regulation of food intake have been performed in animals in which subjective responses cannot be recorded. With regard to satiety, a modulation of hedonic response to food, called "alliesthesia,"¹⁴ has been hypothesized to be controlled by internal nutritional conditions. However, the results of Rolls et al,¹⁵ showing that cyclamate, a nonnutritive sweetener, was nearly as effective as glucose in reducing food intake, would suggest that sensory or cognitive factors are also playing a role in that respect. Our study supports these conclusions.

In animals, adulterating the palatability of foods with quinine both reduces the number and size of the meals.¹⁶ However, in humans, the number of meals frequently depends on social habits, as was the case in our patient.

The influence of a disorder of long-term body weight regulation must also be discussed. An initial weight reduction could be induced for a large part by the disturbance of smell and taste perceptions. However, in animals, hypophagia due to a lower palatability (quinine addition) does not result in a substantial and permanent weight loss¹⁶ because of an escape phenomenon normalizing food intake within a few days. Permanent weight reduction and a shift of the body weight set point has been observed in lateral hypothalamic injury.¹⁷ It could be hypothesized that the dorsomedial thalamic nuclei also play a role in the long-term body weight regulation.

In conclusion, this case confirms a role of the dorsomedial thalamus in the perception of odors and taste and suggests that such perceptions can be altered mainly in their hedonic component. Furthermore, it points out a possible role of hedonic factors in the short-term regulation of food intake and perhaps of the dorsomedial nuclei in the long-term control of body weight.

	Acknowledgments

 
We thank Dr Claude Onckelinck for reviewing the manuscript.

Received July 12, 1996; revision received September 9, 1996; accepted September 16, 1996.

	References

Top Abstract Introduction Case Report Discussion References

 

1. Jones BP, Moskowitz H, Butters N. Olfactory discrimination in alcoholic Korsakoff patients. Neuropsychologia. 1975;13:173-179.[Medline] [Order article via Infotrieve]
2. Jones BP, Butters N, Moskowitz HR, Montgomery K. Olfactory and gustatory capacities of alcoholic Korsakoff patients. Neuropsychologia. 1978;16:332-337.
3. Potter H, Butters NM. An assessment of olfactory deficits in patients with damage to prefrontal lobe. Neuropsychologia. 1980;18:621-628.[Medline] [Order article via Infotrieve]
4. Spreen O, Strauss E. A Compendium of Neuropsychological Tests, Administration, Norms, and Commentary. Oxford, UK: Oxford University Press; 1991.
5. Schaltenbrand G, Wahren W. Atlas for Stereotaxy of the Human Brain. Stuttgart, Germany: Georg Thieme Publishers; 1977.
6. Bogousslavsky J, Regli F, Uske A. Thalamic infarcts: clinical syndromes, etiology, and prognosis. Neurology. 1988;38:837-848.[Abstract/Free Full Text]
7. Rousseaux M. Amnesias following limited thalamic lesions. In: Delacour J, ed. The Memory Systems of the Brain. London, UK: World Scientific; 1994:241-277.
8. Benjamin RM, Jackson JC. Unit discharges in the mediodorsal nucleus of the squirrel monkey evoked by electrical stimulation of the olfactory bulb. Brain Res. 1974;75:181-191.[Medline] [Order article via Infotrieve]
9. Rausch R, Serfetinides EA, Crandall PH. Olfactory memory in patients with anterior lobectomy. Cortex. 1977;13:445-452.[Medline] [Order article via Infotrieve]
10. Eichenbaum H, Morton TH, Potter H, Corkin S. Selective olfactory deficits in case H.M. Brain. 1983;106:459-472.[Abstract/Free Full Text]
11. Schiffman SS, Gatlin CA. Clinical physiology of taste and smell. Ann Rev Nutr. 1993;13:405-436.[Medline] [Order article via Infotrieve]
12. Constantinescu CG, Raps EC, Cohen JA, West SE, Doty RL. Olfactory disturbances as the initial or most prominent symptom of multiple sclerosis. J Neurol Neurosurg Psychiatry. 1994;57:1011-1012.[Medline] [Order article via Infotrieve]
13. Kaiyala K, Woods SC, Schwartz MW. New model for regulation of energy balance and adiposity by the central nervous system. Am J Clin Nutr. 1995;62(suppl 1):1123-1134.
14. Cabanac M. Physiological role of pleasure. Science. 1971;173:1103-1107.[Abstract/Free Full Text]
15. Rolls BJ, Rolls ET, Rowe EA, Sweeney K. Sensory specific satiety in man. Physiol Behav. 1981;27:137-142.[Medline] [Order article via Infotrieve]
16. Sclafani A, Springer D, Kluge L. Effects of quinine adulterated diets on the food intake and body weight of obese and non-obese hypothalamic hyperphagic rats. Physiol Behav. 1976;16:631-640.[Medline] [Order article via Infotrieve]
17. Keesey RE, Boyle PC, Kemnitz JW, Mitchel JS. The role of lateral hypothalamus in determining the body weight set point. In: Novin D, Wyrwicka W, Bray GA, eds. Hunger: Basic Mechanisms and Clinical Implications. New York, NY: Raven Press Publishers; 1976:243-256.

This article has been cited by other articles:

				J. Plailly, J. D. Howard, D. R. Gitelman, and J. A. Gottfried Attention to Odor Modulates Thalamocortical Connectivity in the Human Brain J. Neurosci., May 14, 2008; 28(20): 5257 - 5267. [Abstract] [Full Text] [PDF]

				B N Landis, I Leuchter, D San Millan Ruiz, J-S Lacroix, and T Landis Transient hemiageusia in cerebrovascular lateral pontine lesions J. Neurol. Neurosurg. Psychiatry, May 1, 2006; 77(5): 680 - 683. [Abstract] [Full Text] [PDF]

				J. G. Heckmann, C. Stossel, C. J.G. Lang, B. Neundorfer, B. Tomandl, and T. Hummel Taste Disorders in Acute Stroke: A Prospective Observational Study on Taste Disorders in 102 Stroke Patients Stroke, August 1, 2005; 36(8): 1690 - 1694. [Abstract] [Full Text] [PDF]

				T. M Young and C. J Mathias Taste and Smell Disturbance with the {alpha}-Adrenoceptor Agonist Midodrine Ann. Pharmacother., November 1, 2004; 38(11): 1868 - 1870. [Abstract] [Full Text] [PDF]

This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Rousseaux, M. Articles by Romon, M. Search for Related Content PubMed PubMed Citation Articles by Rousseaux, M. Articles by Romon, M.