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The Journal of Neuroscience, May 14, 2008, 28(20):5257-5267; doi:10.1523/JNEUROSCI.5607-07.2008

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Behavioral/Systems/Cognitive
Attention to Odor Modulates Thalamocortical Connectivity in the Human Brain

Jane Plailly,1 James D. Howard,1 Darren R. Gitelman,1,2,3 and Jay A. Gottfried1,2,4

1Cognitive Neurology and Alzheimer's Disease Center, and 2Departments of Neurology and 3Radiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611, and 4Department of Psychology, Northwestern University Weinberg College of Arts and Sciences, Evanston, Illinois 60208

Correspondence should be addressed to Dr. Jay A. Gottfried, Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, 320 East Superior Street, Searle 11-453, Chicago, IL 60611. Email: j-gottfried{at}northwestern.edu

It is widely assumed that the thalamus is functionally irrelevant for the sense of smell. Although animal studies suggest that the mediodorsal (MD) thalamus links primary olfactory (piriform) cortex to olfactory neocortical projection sites in orbitofrontal cortex (OFC), this transthalamic route is regarded to be inconsequential, particularly compared with a direct monosynaptic pathway linking piriform cortex and OFC. In this study, we combined functional magnetic resonance imaging with novel effective connectivity techniques to measure attention-dependent network coherence within direct (nonthalamic) and indirect (transthalamic) olfactory pathways. Human subjects were presented with (or without) an odor and with (or without) a tone, while selectively attending to either modality. Attention to odor significantly modulated neural coupling within the indirect pathway, strengthening MD thalamus–OFC connectivity. Critically, these effects were modality specific (odor > tone attention), directionally sensitive (forward > backward connections), and selective to route (indirect > direct pathway). Our findings support the idea that the human transthalamic pathway is an active modulatory target of olfactory attention. The results imply that olfaction, like all other sensory modalities, requires a thalamic relay, if only to consciously analyze a smell.

Key words: attention; olfaction; mediodorsal thalamus; fMRI; effective connectivity; dynamic causal modeling; human brain

Received Dec. 18, 2007; revised April 7, 2008; accepted April 10, 2008.

Correspondence should be addressed to Dr. Jay A. Gottfried, Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, 320 East Superior Street, Searle 11-453, Chicago, IL 60611. Email: j-gottfried{at}northwestern.edu






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