Yaara Yeshurun

An Odor is Not Worth a Thousand Words: From Multidimensional Odors to Unidimensional Odor Objects

Olfaction is often referred to as a multidimensional sense. It is multidimensional in that approximately 1000 different receptor types, each tuned to particular odor aspects, together contribute to the olfactory percept. In humans, however, this percept is nearly unidimensional. Humans can detect and discriminate countless odorants, but can identify few by name. The one thing humans can and do invariably say about an odor is whether it is pleasant or not. We argue that this hedonic determination is the key function of olfaction. Thus, the boundaries of an odor object are determined by its pleasantness, which--unlike something material and more like an emotion--remains poorly delineated with words.

Human Tears Contain a Chemosignal

Merely sniffing womens negative emotional tears reduces sexual arousal in men. Emotional tearing is a poorly understood behavior that is considered uniquely human. In mice, tears serve as a chemosignal. We therefore hypothesized that human tears may similarly serve a chemosignaling function. We found that merely sniffing negative-emotion–related odorless tears obtained from women donors induced reductions in sexual appeal attributed by men to pictures of women’s faces. Moreover, after sniffing such tears, men experienced reduced self-rated sexual arousal, reduced physiological measures of arousal, and reduced levels of testosterone. Finally, functional magnetic resonance imaging revealed that sniffing women’s tears selectively reduced activity in brain substrates of sexual arousal in men.

Dynamic reconfiguration of the default mode network during narrative comprehension.

Does the default mode network (DMN) reconfigure to encode information about the changing environment? This question has proven difficult, because patterns of functional connectivity reflect a mixture of stimulus-induced neural processes, intrinsic neural processes and non-neuronal noise. Here we introduce inter-subject functional correlation (ISFC), which isolates stimulus-dependent inter-regional correlations between brains exposed to the same stimulus. During fMRI, we had subjects listen to a real-life auditory narrative and to temporally scrambled versions of the narrative. We used ISFC to isolate correlation patterns within the DMN that were locked to the processing of each narrative segment and specific to its meaning within the narrative context. The momentary configurations of DMN ISFC were highly replicable across groups. Moreover, DMN coupling strength predicted memory of narrative segments. Thus, ISFC opens new avenues for linking brain network dynamics to stimulus features and behaviour.

Sniffing enables communication and environmental control for the severely disabled

Paradoxically, improvements in emergency medicine have increased survival albeit with severe disability ranging from quadriplegia to “locked-in syndrome.” Locked-in syndrome is characterized by intact cognition yet complete paralysis, and hence these individuals are “locked-in” their own body, at best able to communicate using eye blinks alone. Sniffing is a precise sensory-motor acquisition entailing changes in nasal pressure. The fine control of sniffing depends on positioning the soft palate, which is innervated by multiple cranial nerves. This innervation pattern led us to hypothesize that sniffing may remain conserved following severe injury. To test this, we developed a device that measures nasal pressure and converts it into electrical signals. The device enabled sniffs to control an actuator with speed similar to that of a hand using a mouse or joystick. Functional magnetic resonance imaging of device usage revealed a widely distributed neural network, allowing for increased conservation following injury. Also, device usage shared neural substrates with language production, rendering sniffs a promising bypass mode of communication. Indeed, sniffing allowed completely paralyzed locked-in participants to write text and quadriplegic participants to write text and drive an electric wheelchair. We conclude that redirection of sniff motor programs toward alternative functions allows sniffing to provide a control interface that is fast, accurate, robust, and highly conserved following severe injury.

The Privileged Brain Representation of First Olfactory Associations

Authors, poets, and scientists have been fascinated by the strength of childhood olfactory memories. Indeed, in long-term memory, the first odor-to-object association was stronger than subsequent associations of the same odor with other objects. Here we tested the hypothesis that first odor associations enjoy a privileged brain representation. Because emotion impacts memory, we further asked whether the pleasantness of an odor would influence such a representation. On day 1, we associated the same visual objects initially with one, and subsequently with a second, set of pleasant and unpleasant olfactory and auditory stimuli. One week later, we presented the same visual objects and tested odor-associative memory concurrent with functional magnetic resonance brain imaging. We found that the power (% remembered) of early associations was enhanced when they were unpleasant, regardless of whether they were olfactory or auditory. Brain imaging, however, revealed a unique hippocampal activation for early olfactory but not auditory associations, regardless of whether they were pleasant or unpleasant. Activity within the hippocampus on day 1 predicted the olfactory but not auditory associations that would be remembered one week later. These findings confirmed the hypothesis of a privileged brain representation for first olfactory associations.

Spared and impaired olfactory abilities after thalamic lesions.

Olfactory information reaches olfactory cortex without a thalamic relay. This neuroanatomical substrate has combined with functional findings to suggest that, in olfaction, the typical thalamic role in sensory processing has shifted to the olfactory bulb or olfactory cortex. With this in mind, we set out to ask whether the thalamus at all plays a significant functional role in human olfaction. We tested olfactory function in 17 patients with unilateral focal thalamic lesions and in age-matched healthy controls. We found that thalamic lesions did not significantly influence olfactory detection but significantly impaired olfactory identification, and only right lesions altered olfactory hedonics by reducing the pleasantness of pleasant odors. An auditory control revealed that this shift in pleasantness was olfactory specific. These olfactory impairments were evident in explicit measures of perception, as well as in patterns of sniffing. Whereas healthy subjects modulated their sniffs in accordance with odorant content, thalamic patients did not. We conclude that, although the thalamus is not in the path of olfactory information from periphery to cortex, it nevertheless plays a significant functional role in human olfaction.

Working Memory Across Nostrils

Whether olfactory working memory involves verbal representations or neural images of odor per se remains unclear. This study investigated whether verbal representation influences performance in an olfactory delayed-match-to-sample task and used monorhinal presentation to generate hypotheses as to the underlying anatomy of this mechanism. The main findings were that (a) nameable odorants were easier to remember than hard-to-name odorants and (b) the nameability effect was more pronounced when the evaluation was done across nostrils. Considering these results within a proposed model implies dual representation in olfactory working memory: All odors, nameable and hard to name, are represented both perceptually and verbally.

Same Story, Different Story: The Neural Representation of Interpretive Frameworks

Differences in people’s beliefs can substantially impact their interpretation of a series of events. In this functional MRI study, we manipulated subjects’ beliefs, leading two groups of subjects to interpret the same narrative in different ways. We found that responses in higher-order brain areas—including the default-mode network, language areas, and subsets of the mirror neuron system—tended to be similar among people who shared the same interpretation, but different from those of people with an opposing interpretation. Furthermore, the difference in neural responses between the two groups at each moment was correlated with the magnitude of the difference in the interpretation of the narrative. This study demonstrates that brain responses to the same event tend to cluster together among people who share the same views.

The butterfly effect: amplification of local changes along the temporal processing hierarchy

Changing just a few words in a story can induce a substantial change in the overall narrative. How does the brain accumulate and process local and sparse changes, creating a unique situation model of the story, over the course of a real-life narrative? Recently, we mapped a hierarchy of processing timescales in the brain: from early sensory areas that integrate information over 10s-100s ms, to high-order areas that integrate information over many seconds to minutes. Based on this hierarchy, we hypothesize that early sensory areas would be sensitive to local changes in word use, but that there will be increasingly divergent neural responses along the processing hierarchy as higher-order areas accumulate and amplify these local changes. To test this hypothesis, we created two structurally related but interpretively distinct narratives by changing some individual words. We found that the neural response distance between the stories was amplified as story information is transferred from low-level regions (e.g. early auditory cortex) to high-level regions (e.g precuneus and prefrontal cortex) and that the neural difference between stories is highly correlated with an area’s ability to integrate information over time. Our results suggest a neural mechanism by which two similar situations become easy to distinguish.

Amplification of local changes along the timescale processing hierarchy

Significance Changing a few words in a story can drastically alter the interpretation of the narrative. How does the brain amplify sparse changes in word selection to create a unique neural representation for each narrative? In our study, participants listened to one of two stories while being scanned using fMRI. The stories had an identical grammatical structure but varied in a small number of words, resulting in two distinct narratives. We found that differences in neural responses between the stories were amplified as story information was transferred from low-level regions (that are sensitive to the words’ acoustic features) to high-level regions (that accumulate and integrate information across sentences). Our results demonstrate how subtle differences can be accumulated and amplified along the cortical hierarchy. Small changes in word choice can lead to dramatically different interpretations of narratives. How does the brain accumulate and integrate such local changes to construct unique neural representations for different stories? In this study, we created two distinct narratives by changing only a few words in each sentence (e.g., “he” to “she” or “sobbing” to “laughing”) while preserving the grammatical structure across stories. We then measured changes in neural responses between the two stories. We found that differences in neural responses between the two stories gradually increased along the hierarchy of processing timescales. For areas with short integration windows, such as early auditory cortex, the differences in neural responses between the two stories were relatively small. In contrast, in areas with the longest integration windows at the top of the hierarchy, such as the precuneus, temporal parietal junction, and medial frontal cortices, there were large differences in neural responses between stories. Furthermore, this gradual increase in neural differences between the stories was highly correlated with an area’s ability to integrate information over time. Amplification of neural differences did not occur when changes in words did not alter the interpretation of the story (e.g., sobbing to “crying”). Our results demonstrate how subtle differences in words are gradually accumulated and amplified along the cortical hierarchy as the brain constructs a narrative over time.