Memory and Learning: Visually-evoked Olfactory fMRI Activation Patterns and its Dynamics
Prasanna Karunanayaka1, Xin Zhang2, Michael Tobia1, Jianli Wang1, Bin Zhang2, Bin Zhu 2, and Qing Yang1

1Radiology, Penn State University, Hershey, PA, United States, 2The affiliated Drum Tower hospital of Nanjing university medical school, Nanjing, China, People's Republic of

Synopsis

Behavioral studies show that human odor perception is highly dynamic, incorporates both spatial and temporal codes, and is easily influenced by information from other sensory systems such as vision. However, the neural representation of odor perception and its dynamic processing by the brain is poorly understood. In this research, using olfactory task fMRI, we attempt to unravel how olfactory-related neural networks interact in both space and time in order to explore how the olfactory and the visual systems integrate information at the central or perceptual levels in the human brain.

Introduction/Purpose

Odor stimulation strongly influences human memory formation. The role of odors in learning and memory, and the mechanisms by which visual information influence odor-memory formation, however, remains poorly understood [1, 2]. In this study we used neutral visual cues (i.e., symbols “# “and “*”) that were either paired or unpaired with an odor to determine the dynamic pattern of brain activity and connectivity of odor-visual association in the human brain. Using olfactory fMRI and Independent Component Analysis (ICA), we provide new information about the functional circuitry that may be responsible for forming rapid olfactory-visual associations in the human brain [2].

Methods

20 healthy subjects (mean age 25 ± 10 yrs.) took part in the fMRI study at the Gulou Hospital in China with IRB approval. Using the OLFACT™ Computerized Test Battery, the smell identification ability and odor threshold levels of study participants were tested and deemed normal. All participants completed the odor-visual olfactory fMRI paradigm shown in Figure 1. This paradigm was specifically designed to investigate whether an odor-visual association could be established after pairing an odor with a neutral visual cue, i.e., the “#” symbol. An unpaired visual cue, the symbol “*”, was presented randomly during the paradigm. These two symbols were selected because they are not likely to be associated with any semantic or affective attributes of human olfactory function. An MR compatible olfactometer with a flow rate of 8 L/min and synchronized with image acquisition and visual cues was used for stimulus presentation. MR images of the entire brain were acquired using EPI on a Philips 3T scanner with the following parameters: TR / TE / FA= 2000 ms / 30 ms / 90°; FOV = 220 mm x 220 mm; acquisition matrix= 80 x 80, 30 slices; slice thickness= 4 mm, and the number of repetitions= 310. The group ICA analysis was based on FastICA algorithm and performed according to the methods outlined elsewhere [3, 4]. ICA is a data driven method that can generate scale- and statistically-independent spatial patterns of odor-related fMRI activation with unique temporal behavior. Using individual IC time courses, the associated hemodynamic response function (HRF) and the single-trial response of each IC network was evaluated using methods described in Eichele et al. [5].

Results

Figure 2 [(a) and (b)] shows two task-related group IC maps that subserve odor-visual association fMRI paradigm. These IC maps encompass: (a) primary olfactory cortex (POC), amygdala and hippocampus and (b) lingual and fusiform gyri. We quantified the respective IC network responses during odor-visual association in terms of average β estimates as shown in Figure 2c. Both primary olfactory and visual networks showed similar pattern of response decrease during this paradigm (i.e., roughly exponentially decaying). In IC1 and IC2, the differences in β values for encoding and retrieval 1 conditions did not reach statistical significance after correcting for multiple comparisons. However, in both networks, the β values for the encoding conditions were significantly different from retrieval 2 and during conditions where the unpaired visual-cue ‘*’ was presented. Additionally, for IC 1, the β values for encoding were significantly correlated with the β values of the retrieval 1 conditions (r=-0.491517, p< 0.02).

Discussion/Conclusion

Our results demonstrated that a neutral visual-cue, which was previously paired with an odor, can, in fact, evoke BOLD activation in primary olfactory cortex in addition to the primary and associative visual cortex. This process seems to be highly dynamic and rapid in terms of the time-course signal in respective olfactory and visual systems [2]. Our results provide preliminary evidence for odor-visual association because of the negative correlation between encoding β values and retrieval 1 β values. Taken together, these results suggest both a rapid and significant interaction between olfactory by visual processing in the human brain. In turn, this will help ask new questions about multi-sensory integration that were not feasible before.

Acknowledgements

The study was supported by the Department of Radiology at Penn State, George M.Leader Foundation and a grant from the U.S.National Institute of Aging, R01-AG027771

References

[1] Gottfried et al. Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron. 2004; 42(4): p. 687-95.

[2] Karunanayaka et al. Rapidly Acquired Multisensory Association in the Olfactory Cortex. Brain and Beh. 2015.

[3]. Calhoun, V.D. et al. A method for making group inferences from functional MRI data using independent component analysis. HBM. 2001; 14(3): 140-151.

[4]. Karunanayaka et al. Networks involved in olfaction and their dynamics using independent component analysis and unified structural equation modeling. HBM. 2014; 35(5): 2055-2072.

[5]. Eichele et al. Prediction of human errors by maladaptive changes in event-related brain networks. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(16): 6173-6178.

Figures

Figure 1. The olfactory-visual association fMRI Paradigm. In order to offset habituation, each cycle is repeated 2 times with increasing intensity of lavender odorant. During encoding trial conditions, the lavender odorant is paired with the symbol “#”. This symbol is then presented by itself during retrieval 1 and 2 trial conditions. The symbol “*” was never paired with an odorant and the corresponding trials were used as the control condition for comparison.

Figure 2. Two IC maps that subserve odor-visual association: (a) primary olfactory cortex (POC), amygdala and hippocampus and (b) lingual and fusiform gyrus. (c) Network responses in terms of β values.



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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