Temporally‐precise basolateral amygdala activation is required for the formation of taste memories in gustatory cortex

Elor Arieli; Ron Gerbi; Mark Shein‐Idelson; Anan Moran

doi:10.1113/jp280213

Temporally-precise basolateral amygdala activation is required for the formation of taste memories in gustatory cortex

10.1101/2020.03.29.013995 ◽

2020 ◽

Author(s):

Elor Arieli ◽

Ron Gerbi ◽

Mark Shein-Idelson ◽

Anan Moran

Keyword(s):

Basolateral Amygdala ◽

Time Lag ◽

Nucleus Basalis ◽

Electrophysiological Recording ◽

Long Term Memory ◽

Projection Neurons ◽

Dynamic Activity ◽

Gustatory Cortex ◽

Taste Experience

AbstractLearning to associate malaise with the intake of novel food is critical for survival. Since food poisoning may take hours to affect, animals developed brain circuits to transform the current novel taste experience into a taste memory trace (TMT) and bridge this time lag. Ample studies showed that the basolateral amygdala (BLA), the nucleus basalis magnocellularis (NBM) and the gustatory cortex (GC) are involved in TMT formation and taste-malaise association. However, how dynamic activity across these brain regions during novel taste experience promotes the formation of these memories is currently unknown. We used the conditioned taste aversion (CTA) learning paradigm in combination with short-term optogenetics and electrophysiological recording in rats to test the hypothesis that temporally specific activation of BLA projection neurons is essential for TMT formation in the GC, and consequently CTA. We found that late-epoch (LE, >800ms), but not the early epoch (EE, 200-700ms), BLA activation during novel taste experience is essential for normal CTA, for early c-Fos expression in the GC (a marker of TMT formation) and for the subsequent changes in GC ensemble palatability coding. Interestingly, BLA activity was not required for intact taste identity or palatability perceptions. We further show that BLA-LE information is transmitted to GC through the BLA→NBM pathway where it affects the formation of taste memories. These results expose the dependence of long-term memory formation on specific temporal windows during sensory responses and the distributed circuits supporting this dependence.SignificanceConsumption of a novel taste may result in malaise and poses a threat to animals. Since the effects of poisoning appear only hours after consumption, animals must store the novel taste’s information in memory until they associate it with its value (nutritious or poisonous). Here we elucidate the neuronal activity patterns and circuits that support the processing and creation of novel-taste memories in rats. Our results show that specific patterns of temporal activation in the basolateral amygdala transmitted across brain areas are important for formation of taste memory and taste-malaise association. These findings may shed light on long-term activity-to-memory transformation in other sensory modalities.

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Oxytocin enhances basolateral amygdala activation and functional connectivity in autistic women while processing emotional faces

10.31219/osf.io/yjpe9 ◽

2021 ◽

Author(s):

Tanya Procyshyn ◽

MIchael Lombardo ◽

Meng-Chuan Lai ◽

Bonnie Auyeung ◽

Sarah Crockford ◽

...

Keyword(s):

Functional Connectivity ◽

Basolateral Amygdala ◽

Brain Regions ◽

Placebo Condition ◽

Emotional Faces ◽

Amygdala Activation ◽

Within Subjects ◽

Emotional Information Processing ◽

Face Stimuli ◽

The Right

Background: Oxytocin is hypothesized to promote positive social interactions by enhancing the salience of social stimuli, which may be reflected by altered amygdala activation. While previous neuroimaging studies have reported that oxytocin enhances amygdala activation to emotional face stimuli in autistic men, effects in autistic women remain unclear. Methods: The influence of intranasal oxytocin on neural response to emotional faces vs. shapes were tested in 16 autistic and 21 non-autistic women by fMRI in a placebo-controlled, within-subjects, cross-over design. Effects of group (autistic vs. non-autistic) and drug condition (oxytocin vs. placebo) on the activation and functional connectivity of the basolateral amygdala, the brain’s “salience detector”, were assessed. Relationships between individual differences in autistic-like traits, social anxiety, salivary oxytocin levels, and amygdala activation were also explored.Results: Autistic and non-autistic women showed minimal activation differences in the placebo condition. Significant drug × group interactions were observed for both amygdala activation and functional connectivity. Oxytocin increased left basolateral amygdala activation among autistic women (35 voxel cluster, MNI coordinates of peak voxel = -22 -10 -28; mean change=+0.079%, t=3.159, ptukey=0.0166), but not non-autistic women (mean change =+0.003%, t=0.153, ptukey=0.999). Furthermore, oxytocin increased functional connectivity of the right basolateral amygdala with brain regions associated with socio-emotional information processing in autistic women, but not non-autistic women, thereby attenuating group connectivity differences observed in the placebo condition. Conclusions: This work demonstrates that intranasal oxytocin increases basolateral amygdala activation and connectivity in autistic women while processing emotional faces, which extends and specifies previous findings in autistic men.

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Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

10.1101/2020.12.02.406900 ◽

2020 ◽

Author(s):

Jian-You Lin ◽

Narendra Mukherjee ◽

Max J. Bernstein ◽

Donald B. Katz

Keyword(s):

Basolateral Amygdala ◽

Neural Responses ◽

Response Dynamics ◽

Related Activity ◽

Gustatory Cortex ◽

Laser Illumination ◽

Consumption Decisions ◽

Cortical Projections ◽

Optical Fiber Probes ◽

Oral Presentations

ABSTRACTTaste palatability is centrally involved in consumption decisions—we ingest foods that taste good and reject those that don’t. Gustatory cortex (GC) and basolateral amygdala (BLA) almost certainly work together to mediate palatability-driven behavior, but the precise nature of their interplay during taste decision-making is still unknown. Here, we take a step toward filling this gap in our knowledge, by investigating the specific role that activity in the BLA→GC pathway plays in the emergence of palatability-related firing in GC response dynamics (which influence consumption decisions). We implanted electrode/optical-fiber probes in virally-prepared female Long-Evans rats, such that we could optogenetically hyperpolarize BLA→GC axons, perturbing activity in these axons without affecting BLA and GC somas, while recording GC neural responses to intra-oral presentations of a diverse taste battery. This inter-regional axonal perturbation strongly altered GC taste responses, but despite the laser illumination being tonic for the first 2s that the taste was on the tongue, the alterations were far from monolithic: rather than changing all moments of the response equally, or causing a simple exponential decay of changes, the perturbation was most strongly felt at the onset times of previously-described response epochs; furthermore, the effect was epoch-specific—perturbations had little impact on the amount of taste identity information in the “middle epoch” of the responses, but reduced evidence of palatability-related activity in the “late-epoch.” Finally, BLA→GC axon inhibition affected the nature of the epochal dynamics themselves, such that the normal abruptness of the behaviorally-relevant ensemble transitions into the palatability-related epoch was greatly diminished. These results suggest that BLA “organizes” behavior-related GC taste dynamics.

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Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

eLife ◽

10.7554/elife.65766 ◽

2021 ◽

Vol 10 ◽

Author(s):

Jian-You Lin ◽

Narendra Mukherjee ◽

Max J Bernstein ◽

Donald B Katz

Keyword(s):

Decision Making ◽

Basolateral Amygdala ◽

Response Dynamics ◽

Related Activity ◽

Gustatory Cortex ◽

Identity Information ◽

Precise Nature ◽

Consumption Decisions ◽

Taste Response ◽

Cortical Projections

Taste palatability is centrally involved in consumption decisions—we ingest foods that taste good and reject those that don't. Gustatory cortex (GC) and basolateral amygdala (BLA) almost certainly work together to mediate palatability-driven behavior, but the precise nature of their interplay during taste decision-making is still unknown. To probe this issue, we discretely perturbed (with optogenetics) activity in rats’ BLA→GC axons during taste deliveries. This perturbation strongly altered GC taste responses, but while the perturbation itself was tonic (2.5 s), the alterations were not—changes preferentially aligned with the onset times of previously-described taste response epochs, and reduced evidence of palatability-related activity in the ‘late-epoch’ of the responses without reducing the amount of taste identity information available in the ‘middle epoch.’ Finally, BLA→GC perturbations changed behavior-linked taste response dynamics themselves, distinctively diminishing the abruptness of ensemble transitions into the late epoch. These results suggest that BLA ‘organizes’ behavior-related GC taste dynamics.

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