Functional mapping of cerebral odor processing

Journal of Neurophysiology, 2012

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Human Brain Mapping, 2007

Discriminating between successively presented odors requires brief storage of the first odor's perceptual trace, which then needs to be subsequently compared to the second odor in the pair. This study explores the cortical areas involved in odor discrimination and compares them with findings from studies of working-memory, traditionally investigated with n-back paradigms. Sixteen right-handed subjects underwent H215O positron emission tomography during counterbalanced conditions of odorless sniffing, repeated single odor detection, multiple odor detection, and conscious successive discrimination between odor pairs. Eight odorants were delivered using a computer-controlled olfactometer through a birhinal nasal cannula. Conscious successive odor discrimination evoked significantly greater activity in the left anterior insula and frontopolar gyrus when compared to reported sensory detection of the identical odors. Additional activation was found in the left lateral orbital/inferior frontal and middle frontal gyri when discrimination was compared to the odorless condition. The left anterior insula is likely involved in the evaluation of odor properties. Consistent with other studies, frontopolar and middle frontal gyrus activation is more likely related to working memory during odor discrimination. Hum Brain Mapp, 2007. © 2006 Wiley-Liss, Inc.

Fukuda. Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol 84: 1656 -1666, 2000. This study describes the functional anatomy of olfactory and visual naming and matching in humans, using positron emission tomography (PET). One baseline control task without olfactory or visual stimulation, one control task with simple olfactory and visual stimulation without cognition, one set of olfactory and visual naming tasks, and one set of olfactory and visual matching tasks were administered to eight normal volunteers. In the olfactory naming task (ON), odors from familiar items, associated with some verbal label, were to be named. Hence, it required long-term olfactory memory retrieval for stimulus recognition. The olfactory matching task (OM) involved differentiating a recently encoded unfamiliar odor from a sequentially presented group of unfamiliar odors. This required short-term olfactory memory retrieval for stimulus differentiation. The simple olfactory and visual stimulation resulted in activation of the left orbitofrontal region, the right piriform cortex, and the bilateral occipital cortex. During olfactory naming, activation was detected in the left cuneus, the right anterior cingulate gyrus, the left insula, and the cerebellum bilaterally. It appears that the effort to identify the origin of an odor involved semantic analysis and some degree of mental imagery. During olfactory matching, activation was observed in the left cuneus and the cerebellum bilaterally. This identified the brain areas activated during differentiation of one unlabeled odor from the others. In cross-task analysis, the region found to be specific for olfactory naming was the left cuneus. Our results show definite recruitment of the visual cortex in ON and OM tasks, most likely related to imagery component of these tasks. The cerebellar role in cognitive tasks has been recognized, but this is the first PET study that suggests that the human cerebellum may have a role in cognitive olfactory processing as well.

Journal of Cognitive Neuroscience, 1999

n The functional anatomy of perceptual and semantic processings for odors was studied using positron emission tom ography (PET). The rst experim ent was a pretest in which 71 normal subjects were asked to rate 185 odorants in terms of inten sity, familiarity, hedonicity, and com estibility and to name the odorants. This pretest was necessary to select the most appropriate stim uli for the different cognitive tasks of the secon d experim ent. The second one was a PET exper iment in which 15 normal subjects were scanned using the water bolus method to measure regional cerebral blood ow (rCBF) during the performance in three conditio ns. In the rst (perceptual) condition, subjects were asked to judge whether an odor was familiar or not. In the secon d (semantic) con dition, subjects had to decide whether an odor corresponded to a com estible item or not. In the third (detection) conditio n, subjects had to judge w hether the perceived stimulus was m ade of an odor or was just air. It was hypoth etized that the three tasks were hierarchically organized from a super cial detectio n level to a deep semantic level. O dorants were presented with an air-ow olfactom eter, which allowed the stimulations to be synchronized w ith breathing. Subtraction of activation images obtain ed between familiarity and control judgm ents revealed that familiarity judgm ents were mainly associated with the activity of the right orbito-frontal area, the subcallosal gyrus, the left inferior frontal gyrus, the left superior frontal gyrus, and the anterior cingulate (Brodm ann's areas 11, 25, 47, 9, and 32, respectively). The com estibility minus familiarity com parison showed that com estibility judgm ents selectively activated the primary visual areas. In contrast, a decrease in rCBF was observed in these same visual areas for familiarity judgm ents and in the orbitofrontal area for com estibility judgm ents. These results suggest that orbito-frontal and visual regions interact in odor processing in a com plem entary way, depending on the task requirements. n

NeuroImage, 2001

Humans routinely make judgments about olfactory stimuli. However, few studies have examined the functional neuroanatomy underlying the cognitive operations involved in such judgments. In order to delineate this functional anatomy, we asked 12 normal subjects to perform different judgments about olfactory stimuli while regional cerebral blood flow (rCBF) was measured with PET. In separate conditions, subjects made judgments about the presence (odor detection), intensity, hedonicity, familiarity, or edibility of different odorants. An auditory task served as a control condition. All five olfactory tasks induced rCBF increases in the right orbitofrontal cortex (OFC), but right OFC activity was highest during familiarity judgments and lowest during the detection task. Left OFC activity increased significantly during hedonic and familiarity judgments, but not during other odor judgments. Left OFC activity was significantly higher during hedonicity judgments than during familiarity or other olfactory judgments. These data demonstrate that aspects of odor processing in the OFC are lateralized depending on the type of olfactory task. They support a model of parallel processing in the left and right OFC in which the relative level of activation depends on whether the judgment involves odor recognition or emotion. Primary visual areas also demonstrated a differential involvement in olfactory processing depending on the type of olfactory task: significant rCBF increases were observed in hedonic and edibility judgments, whereas no significant rCBF increases were found in the other three judgments. These data indicate that judgments of hedonicity and edibility engage circuits involved in visual processing, but detection, intensity, and familiarity judgments do not.

Neuron, 2000

fibers connect to mitral and tufted cells of the olfactory bulb, which via the olfactory tract and tubercle projects † Department of Neurology ‡ Department of Clinical Neuroscience (Neurotech) to the olfactory cortex (Powell et al., 1965). The olfactory cortex in higher mammals comprises the anterior olfac-Karolinska Institute Berzelisvä g 3 tory nucleus and the piriform, periamygdaloid, and transentorhinal cortices (Powell et al., 1965). The olfac-171 77 Stockholm Sweden tory tract also connects directly to the periamygdaloid cortex, and the olfactory tubercle to the mediodorsal § Department of Psychology Uppsala University thalamic nucleus (Powell et al., 1965; Morecraft et al., 1992). From the olfactory cortex and amygdala, the third 751 42 Uppsala Sweden neuron reaches targets in the orbitofrontal cortex, subiculum, thalamus, hypothalamus, brainstem, and caudate nucleus (Powell et al., 1965; Morecraft et al., 1992). The olfactory structures have recently been mapped in Summary humans. Studies with PET and functional MR indicate that passive smelling of odors activates the amygdala-How the human brain processes the perception, dispiriform cortex, the right orbitofrontal cortex, and the crimination, and recognition of odors has not been insular-periinsular cortex (Zatorre et al., 1992; Simsystematically explored. Cerebral activations were monds et al., 1997; Williams et al., 1997; Zald and Pardo, therefore studied with PET during five different olfac-1997; Sobel et al., 1998a, 1998b). In addition, a cerebellar tory tasks: monorhinal smelling of odorless air (AS), activation has been reported by Sobel et al. (1998a, single odors (OS), discrimination of odor intensity 1998b). The exact subset of structures involved seems (OD-i), discrimination of odor quality (OD-q), and odor to vary with the particular odor used (Simmonds et al., recognition memory (OM). OS activated amygdala-pir-1997; Williams et al., 1997; Zald and Pardo, 1997). Lesion iform, orbitofrontal, insular, and cingulate cortices and studies suggest that the engaged structures also vary right thalamus. OD-i and OD-q both engaged left insula with the particular odor-associated function, as reported and right cerebellum. OD-q also involved other areas, in patients with mesial temporal lobe epilepsy (Zatorre including right caudate and subiculum. OM did not and Jones-Gotman, 1991; Jones-Gotman and Zatorre, activate the insula, but instead, the piriform cortex. 1993; Savic et al., 1997). For example, patient H. M., With the exception of caudate and subiculum, it shared

The Journal of Neuroscience, 2000

The orbitofrontal cortex (OF) is strongly and reciprocally connected with the perirhinal (PR) and entorhinal areas of the medial temporal lobe and plays an important role in odor recognition memory. This study characterized firing patterns of single neurons in the OF of rats performing a continuous odor-guided delayed nonmatch to sample (DNMS) task. Most OF neurons fired in association with one or more task events, including the initiation of trials, the sampling of odor stimuli, and the consumption of rewards. OF neurons also exhibited sustained odorselective activity during the memory delay, and a large proportion of OF cells had odor-specific enhanced or suppressed responses on stimulus repetition. Most OF neurons were activated during several task events, or associated with complex behavioral states. The incidence of cells that fired in association with the critical match/non-match judgement was increased as the DNMS rule was learned, and was higher in OF than in perirhinal and entorhinal cortex. Furthermore, the classification of match and nonmatch trials was correlated with accuracy in performance of that judgement. These findings are consistent with the view that OF is a high order association cortex that plays a role both in the memory representations for specific stimuli and in the acquisition and application of task rules.

Psychonomic Bulletin & Review, 1996

Neuron, 2011

Natural odors, generally composed of many monomolecular components, are analyzed by peripheral receptors into component features and translated into spatiotemporal patterns of neural activity in the olfactory bulb. Here, we will discuss the role of the olfactory cortex in the recognition, separation and completion of those odor-evoked patterns, and how these processes contribute to odor perception. Recent findings regarding the neural architecture, physiology, and plasticity of the olfactory cortex, principally the piriform cortex, will be described in the context of how this paleocortical structure creates odor objects.

NeuroImage, 2005

We used positron emission tomography (PET) to investigate brain regions associated with odor imagery. Changes in regional cerebral blood flow (CBF) during odor imagery were compared with changes during nonspecific expectation of olfactory stimuli and with those during odor perception. Sixty-seven healthy volunteers were screened for their odor imagery (with a paradigm developed in a previous study), and 12 of them, assessed to be bgood odor imagers,Q participated in the neuroimaging part of the study. Imagination of odors was associated with increased activation in several olfactory regions in the brain: the left primary olfactory cortical (POC) region including piriform cortex, the left secondary olfactory cortex or posterior orbitofrontal cortex (OFC), and the rostral insula bilaterally. Furthermore, blood flow in two regions within the right orbitofrontal cortex correlated significantly with the behavioral measure of odor imagery during scanning. Overall, the findings indicated that neural networks engaged during odor perception and imagery overlap partially.