Abstract
It is widely assumed that the thalamus is not involved in olfaction. The ventrolateral thalamus is, however, closely connected to the contralateral cerebellum, which is involved in the sense of smell based on findings from functional imaging studies and findings of olfactory deficits in patients with cerebellar disease. We hypothesized that olfactory deficits following lesions of the ventrolateral thalamus may be similar to olfactory deficits following cerebellar lesions. Fifteen patients with a focal thalamic lesion involving the ventrolateral thalamus were examined and compared to 15 patients with a focal cerebellar lesion and 15 healthy controls. A detailed olfactory test (“Sniffin’ Sticks”) was used to assess different olfactory functions separately for each nostril. In the group of patients with a lesion of the ventrolateral thalamus, an impairment of the odor threshold was found at the ipsilateral nostril, consistent with the unilateral orientation of the olfactory system in the telencephalon. In the group of patients with a cerebellar lesion, an olfactory deficit at the contralesional nostril emerged. In controls, no significant side difference was found. The involvement of the ventrolateral thalamus in olfaction is comparable to that of the cerebellum in respect to odor threshold. Further study is needed to assess if these findings are related to an impairment of an olfactomotor loop. Present evidence for this hypothesis is indirect. Effects were subclinical as none of the patients reported olfactory disturbance. The results suggest that the cerebello-thalamic axis plays an adjuvant role in olfaction.
Similar content being viewed by others
References
Schünke M, Schulte E (2006) Prometheus – Kopf und Neuroanatomie. Thieme, Stuttgart
Kay LM, Sherman SM (2007) An argument for an olfactory thalamus. Trends Neurosci 30:47–53
Gottfried JA (2006) Smell: central nervous processing. In: Hummel T, Welge-Lüssen A (eds) Taste and smell. An update. Adv Otorhinolaryngol, vol 63. Karger, Basel, pp 44–69
Motokizawa F (1974) Olfactory input to the thalamus: electrophysiological evidence. Brain Res 67:334–337
Price JL (1985) Beyond the primary olfactory cortex: olfactory-related areas in the neocortex, thalamus and hypothalamus. Chem Senses 10:239–258
Plailly J, Howard JD, Gitelman DR, Gottfried JA (2008) Attention to odor modulates thalamocortical connectivity in the human brain. J Neurosci 28:5257–5267
Potter H, Butters N (1980) An assessment of olfactory deficits in patients with damage to prefrontal cortex. Neuropsychologia 18:621–628
Rousseaux M, Muller P, Gahide I, Mottin Y, Romon M (1996) Disorders of smell, taste, and food intake in a patient with a dorsomedial thalamic infarct. Stroke 27:2328–2330
Tham WW, Stevenson RJ, Miller LA (2009) The functional role of the medio dorsal thalamic nucleus in olfaction. Brain Res Rev 62:109–126
Sobel N, Prabhakaran V, Hartley CA et al (1998) Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci 18:8990–9001
Ferdon S, Murphy C (2003) The cerebellum and olfaction in the aging brain: a functional magnetic resonance imaging study. Neuroimage 20:12–21
Yousem DM, Williams SC, Howard RO et al (1997) Functional MR imaging during odor stimulation: preliminary data. Radiology 204:833–838
Qureshy A, Kawashima R, Imran MB et al (2000) Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol 84:1656–1666
Abele M, Riet A, Hummel T, Klockgether T, Wüllner U (2003) Olfactory dysfunction in cerebellar ataxia and multiple system atrophy. J Neurol 250:1453–1455
Connelly T, Farmer JM, Lynch DR, Doty RL (2003) Olfactory dysfunction in degenerative ataxias. J Neurol Neurosurg Psychiatry 74:1435–1437
Mainland JD, Johnson BN, Khan R, Ivry RB, Sobel N (2005) Olfactory impairments in patients with unilateral cerebellar lesions are selective to inputs from the contralesional nostril. J Neurosci 6:6362–6371
Stanton GB (1980) Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: an anterograde degeneration study. J Comp Neurol 190:699–731
Sakai ST, Inase M, Tanji J (1996) Comparison of cerebellothalamic and pallidothalamic projections in the monkey (Macaca fuscata): a double anterograde labeling study. J Comp Neurol 368:215–228
Krack P, Dostrovsky J, Ilinsky I et al (2002) Surgery of the motor thalamus: problems with the present nomenclatures. Mov Disord 17:S2–S8
Bastian AJ, Thach WT (1995) Cerebellar outflow lesions: a comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus. Ann Neurol 38:881–892
Melo TP, Bogousslavsky J, Moulin T, Nader J, Regli F (1992) Thalamic ataxia. J Neurol 239:331–337
Solomon DH, Barohn RJ, Bazan C, Grissom J (1994) The thalamic ataxia syndrome. Neurology 44:810–814
Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22:39–52
Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 264:237–243
Härting H, Markowitsch HJ, Neufeld H, Calabrese P, Deisinger K, Kessler J (2000) Wechsler Gedächtnistest–Revidierte Fassung. Hans Huber, Bern
Lehrl S (2005) Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Spitta Verlag, Balingen
Cosson A, Tatu L, Vuillier F, Parratte B, Diop M, Monnier G (2003) Arterial vascularization of the human thalamus: extra-parenchymal arterial groups. Surg Radiol Anat 25:408–415
Lascano AM, Hummel T, Lacroix JS, Landis BN, Michel CM (2010) Spatio-temporal dynamics of olfactory processing in the human brain: an event-related source imaging study. Neuroscience (in press)
Bower JM (1997) Control of sensory data acquisition. Int Rev Neurobiol 41:489–513
Johnson BN, Mainland JD, Sobel N (2003) Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol 90:1084–1094
Ikai Y, Takada M, Shinonaga Y, Mizuno N (1992) Dopaminergic and non-dopaminergic neurons in the ventral tegmental area of the rat project, respectively, to the cerebellar cortex and deep cerebellar nuclei. Neuroscience 51:719–728
Yatim N, Billig I, Compoint C, Buisseret P, Buisseret-Delmas C (1996) Trigeminocerebellar and trigemino-olivary projections in rats. Neurosci Res 25:267–283
Darian-Smith C, Darian-Smith I, Cheema SS (1990) Thalamic projections to sensorimotor cortex in the macaque monkey: use of multiple retrograde fluorescent tracers. J Comp Neurol 299:17–46
Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250
Colebatch JG, Adams L, Murphy K et al (1991) Regional cerebral blood flow during volitional breathing in man. J Physiol 443:91–103
Laing DG (1983) Natural sniffing gives optimum odour perception for humans. Perception 12:99–117
Hummel T, Kobal G (2001) Olfactory event-related potentials. In: Simon SA, Nicolelis MAL (eds) Methods and frontiers in chemosensory research. CRC Press, Boca Raton, pp 429–464
Newman PP, Reza H (1979) Functional relationships between the hippocampus and the cerebellum: an electrophysiological study of the cat. J Physiol 287:405–426
Oganesian EA, Melik-Musian AB, Fanardzhian VV, IuKh Grigorian (1980) Morpho-functional analysis of the nature of cerebello-hippocampal connections. Fiziol Zh SSSR Im I M Sechenova 66:1632–1639
Konczak J, Schoch B, Dimitrova A, Gizewski E, Timmann D (2005) Functional recovery of children and adolescents after cerebellar tumour resection. Brain 128:128–1441
Miller Fischer C (1978) Thalamic pure sensory stroke: a pathologic study. Neurology 28:1141–1144
Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain. Thieme, Stuttgart
Acknowledgments
This project was supported by the START-Program, Faculty of Medicine, RWTH Aachen. We thank Professor Dr. Willmes (Division of Neuropsychology, RWTH Aachen) for his statistical advice. Additionally, we thank Professor Coenen (Division of Neurosurgery, University Bonn) for critical comments on the imaging data.
Conflict of interest statement
There are no conflicts of interest to be disclosed.
Author information
Authors and Affiliations
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zobel, S., Hummel, T., Ilgner, J. et al. Involvement of the human ventrolateral thalamus in olfaction. J Neurol 257, 2037–2043 (2010). https://doi.org/10.1007/s00415-010-5656-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-010-5656-7