In addition to the multisensory evoked responses, functional coupling between aPCX and A1 was enhanced, as assessed with LFP coherence and phase locking. Importantly, both the evoked responses and the functional connectivity changes were only expressed while the rats were in the operant chamber, and not expressed when in their homecage. These results contribute to our understanding of multisensory processing effects in olfaction. Recognizing and identifying odors relies on effectively using predictive cues from other senses e.
Integration of matching non-olfactory and olfactory cues is assessed in common clinical olfactory assessments Doty et al.
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By definition, these appear to be multisensory evoked responses in classically unimodal cortices. In fact, links between the auditory and olfactory cortex in rodents have been well described Budinger et al ; Budinger and Scheich ; Wesson and Wilson However alternative mechanisms of multi-sensory evoked responses in A1 and aPCX are possible. For example, responses need not be directly driven by sensory afferents to the cortex itself, but rather could reflect changes in activity due to very indirect or even neuromodulatory circuits.
For example, the temporal structure of PCX unit activity is shaped by locus coeruleus activation, causing unit firing to be more strongly in phase with respiration Bouret and Sara, Thus, activation of the locus coeruleus, for example, by an alerting stimulus like foot shock, could evoke a change in PCX activity that was not truly a somatosensory evoked response, but rather a more general response to a change in neuromodulatory tone.
A role for involvement of neuromodulatory inputs in shaping the observed multisensory responses is further supported by the fact that they were context-dependent. The change in context could modify attention or alertness, which can directly modify sensory-evoked responses in the olfactory Carlson et al.
Thus, it is difficult to distinguish between changes in context or changes in state as the driver of these effects. Further work is necessary to explore the underlying mechanisms of these learned and context-dependent multisensory responses. In addition to the learned multisensory-evoked responses, functional connectivity between A1 and aPCX was also enhanced in a learning- and context-dependent manner. This effect was apparent using either LFP coherence over long s periods of time while the animal engaged in the task, or in trial-related phase-locking analyses PLI.
Given that the learned change in A1—aPCX functional connectivity was context-dependent suggests that stable synaptic plasticity, such as long-term potentiation, is not a primary mechanism. Rather, the data suggest a flexibility in multisensory processing, where under specific conditions sensory systems are more likely to function coherently, while a change in conditions allows them isolate from each other. Similar context-dependent expression of learned changes in network connectivity have been previously reported within the olfactory cortex itself Cohen et al.
However, enhanced functional connectivity at low frequencies could contribute to local high frequency activity via cross-frequency coupling in the two regions, although this requires further investigation Hyafil et al. Our LFP coherence measures peaked in a similar low frequency range but were present both while the animals were actively engaged in the task and when they specifically were not, and instead were generally grooming or exploring.
This would argue that active sniffing 6—9 Hz; Kepecs et al. Furthermore, in humans performing an auditory-word-cued odor-matching task, high auditory-olfactory cortex coupling during the task was not respiration-dependent Zhou et al. However, respiration has been shown to be important for linking activity within broad networks beyond the olfactory system in both humans Zelano et al. Finally, while odor detection and discrimination can be disrupted in a variety of disorders, odor identification, the linking of an odor sensation with a symbolic label, is generally most vulnerable to pathology associated with dementia Murphy, ; Devanand et al.
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Similarly, animal models of dementia and dementia risk factors often show no deficits in odor discrimination Vloeberghs et al. More complex animal model tasks, such as the auditory-olfactory associative learning task characterized here, may more closely model multisensory links between olfaction and language that are so vulnerable in humans. This is an open-access article distributed under the terms of the Creative Commons Attribution 4. Decisions are customarily a result of the Reviewing Editor and the peer reviewers coming together and discussing their recommendations until a consensus is reached.
When revisions are invited, a fact-based synthesis statement explaining their decision and outlining what is needed to prepare a revision will be listed below. The following reviewer s agreed to reveal their identity: Michael Baum.
Effects of odor on emotion, with implications
Both reviewers found your work potentially interesting and an advance to the field. However, there are some concerns regarding the description of the methods and presentation of the results. Please pay in particularly attention to the comments of reviewer 1 when revising your paper. Finally, please explain why the number of rats used is varying between the experiments.
This work addresses the importance of context and task engagement in a multisensory integration process acquired through learning. To my opinion, this study could provide a valuable advance in the field. It confirms learning-induced changes in electrophysiological activity of each involved sensory areas and addresses for the first time the impact of the experimental context and subject engagement in the task on functional connectivity between these two cortices in response to the same stimulus.
However, in the present way, the manuscript suffers from a lot of imprecisions and need to be thoroughly improved to be really convincing.
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This section is not precise enough and the part on signal processing need to be reorganized in a more rigorous way. For example, it is not clear how baseline LFP activity was determined both in the experimental cage and in the home cage. This point is critical as everything is then corrected by this baseline. Please provide a clear description of how baseline was selected and how the correction was applied. There is a clear discrepancy in the description of these two methods and the detailed part on functional connectivity. I do not understand the reason why the authors divide their group in two instead of using each rat as its own control.
The same lack of precision is also detrimental to results presentation. It is very difficult to follow What is the relation between this two figures? The comparison of the odor response seems to me strange and I am just wondering if there is not an inversion in the results between the two figures and the two structures since activity of the PCx in the beta band is lower than the A1 whereas the graph is showing an inverse result Figure 7: To understand this figure it is really necessary to know more about how the selection of portion of signals where made in the disengaged situation.
Figure 8: How many trials for each animal? This should be indicated close to each figure. On this figure the significant clusters for OT9 seem to be quite different From the three others negative value of the Z score, in a clear different frequency band: 8 Hz instead of between 1 and 2 Hz. I would suggest that this section include a first paragraph with a synthesis of the experimental results and an attempt to relate the power analysis and the functional connectivity study. Then the authors should stay in the line of their data to discuss more the results they obtained.see
5.4 Tasting, Smelling, and Touching
For example, the fact that beta oscillations are context dependent in well trained animals but did not seem to be coherent between the two structures even if nothing is said about PLI in this band. The present study appears to have been carefully conducted, and the results have been appropriately analyzed and graphically portrayed in a clear manner. The manuscript is also very well written and includes an appropriate, conservative discussion of the relevant literature.
The results establish a behavioral model system for future studies of the mechanism whereby the observed linkage of the A1 and aPCX responses is established. As the authors point out in the Discussion Lf , their new auditory-olfactory associative learning task in rats may be a useful model system in which to study the underlying mechanism whereby dementia disrupts the linkage between auditory signals e.
Minor changes: Mention when appropriate in Fig. We are excited that the reviewers and editors found our manuscript to be of interest for publication in eNeuro. Encouraged by these comments, we have carefully considered the limitations of our submitted work, in order to strengthen the manuscript further. Below, we make a point-by-point response in blue font to each reviewer comment.
The revised manuscript includes new text in yellow highlight. We hope that our efforts have made the manuscript acceptable for publication, and we are looking forward to your response. Same comment for the section on spectral coherence. Baseline adjustment procedure is now explained at three occasions on page 5. We hope that the reviewer feels that our methods are now presented with enough clarity. Nonetheless, we have added additional detail where possible to help clarify differences between coherence analyses during trial-based activity and disengagement, and between homecage and operant chamber activity.
We feel that the revised methods section is well balanced with regards to brevity, conciseness and need for methodological detail. Data from these animals were not considered further. As explained in the methods, unfortunately due to technical limitations were were unable to record from the same animals during the entire training regime wich lasted several weeks.
We believe that the increased sample size is sufficient for statistical comparison. We have clarified that Naive control recording data for analysis were taken from animals in their first training sessions when they were still performing at chance levels page 9 and Fig. Data used for analyses are processed as described elsewhere.
We have now clarified that Fig. The data have been updated since we doubled the n in this group. We do not see the inversion the reviewer notes, though now that we have changed the color scheme, the relationship will be more obvious.
We have also changed the color scheme for Fig. We have now clarfied in the figure caption that activity was quantified 1 during the ms of tone presentation tone-evoked activity, 2 for ms starting at tone offset and odor onset odor evoked activity and 3 during ms of tone when the animals were in their home cage passibve tone evoked activity. All animals displayed periods of task-activity intermixed with periods of disengagement from the task, periods where they were mostly grooming.