Amygdala neuronal ensembles dynamically encode behavioral states

2018 ◽  
Author(s):  
Jan Gründemann ◽  
Yael Bitterman ◽  
Tingjia Lu ◽  
Sabine Krabbe ◽  
Benjamin F. Grewe ◽  
...  

AbstractInternal states, including affective or homeostatic states, are important behavioral motivators. The amygdala is a key brain region involved in the regulation of motivated behaviors, yet how distinct internal states are represented in amygdala circuits is unknown. Here, by imaging somatic neural calcium dynamics in freely moving mice, we identify changes in the relative activity levels of two major, non-overlapping populations of principal neurons in the basal nucleus of the amygdala (BA) that predict switches between exploratory and non-exploratory (defensive, anxiety-like) behavioral states across different environments. Moreover, the amygdala widely broadcasts internal state information via several output pathways to larger brain networks, and sensory responses in BA occur independently of behavioral state encoding. Thus, the brain processes external stimuli and internal states in an orthogonal manner, which may facilitate rapid and flexible selection of appropriate, state-dependent behavioral responses.

Science ◽  
2019 ◽  
Vol 364 (6437) ◽  
pp. eaav8736 ◽  
Author(s):  
Jan Gründemann ◽  
Yael Bitterman ◽  
Tingjia Lu ◽  
Sabine Krabbe ◽  
Benjamin F. Grewe ◽  
...  

Internal states, including affective or homeostatic states, are important behavioral motivators. The amygdala regulates motivated behaviors, yet how distinct states are represented in amygdala circuits is unknown. By longitudinally imaging neural calcium dynamics in freely moving mice across different environments, we identified opponent changes in activity levels of two major, nonoverlapping populations of basal amygdala principal neurons. This population signature does not report global anxiety but predicts switches between exploratory and nonexploratory, defensive states. Moreover, the amygdala separately processes external stimuli and internal states and broadcasts state information via several output pathways to larger brain networks. Our findings extend the concept of thalamocortical “brain-state” coding to include affective and exploratory states and provide an entry point into the state dependency of brain function and behavior in defined circuits.


2019 ◽  
Author(s):  
Lisa Voelker ◽  
Bishal Upadhyaya ◽  
Denise M. Ferkey ◽  
Sarah Woldemariam ◽  
Noelle D. L’Etoile ◽  
...  

AbstractIn order to respond to changing environments and fluctuations in internal states, animals adjust their behavior through diverse neuromodulatory mechanisms. In this study we show that electrical synapses between the ASH primary quinine-detecting sensory neurons and the neighboring ASK neurons are required for modulating the aversive response to the bitter tastant quinine in C. elegans. Mutant worms that lack the electrical synapse proteins INX-18 and INX-19 become hypersensitive to dilute quinine. Cell-specific rescue experiments indicate that inx-18 operates in ASK while inx-19 is required in both ASK and ASH for proper quinine sensitivity. Imaging analyses find that INX-19 in ASK and ASH localizes to the same regions in the nerve ring, suggesting that both sides of ASK-ASH electrical synapses contain INX-19. While inx-18 and inx-19 mutant animals have a similar behavioral phenotype, several lines of evidence suggest the proteins encoded by these genes play different roles in modulating the aversive quinine response. First, INX-18 and INX-19 localize to different regions of the nerve ring, indicating that they are not present in the same synapses. Second, removing inx-18 disrupts the distribution of INX-19, while removing inx-19 does not alter INX-18 localization. Finally, by using a fluorescent cGMP reporter, we find that INX-18 and INX-19 have distinct roles in establishing cGMP levels in ASK and ASH. Together, these results demonstrate that electrical synapses containing INX-18 and INX-19 facilitate modulation of ASH nociceptive signaling. Our findings support the idea that a network of electrical synapses mediates cGMP exchange between neurons, enabling modulation of sensory responses and behavior.Author SummaryAnimals are constantly adjusting their behavior to respond to changes in the environment or to their internal state. This behavior modulation is achieved by altering the activity of neurons and circuits through a variety of neuroplasticity mechanisms. Chemical synapses are known to impact neuroplasticity in several different ways, but the diversity of mechanisms by which electrical synapses contribute is still being investigated. Electrical synapses are specialized sites of connection between neurons where ions and small signaling molecules can pass directly from one cell to the next. By passing small molecules through electrical synapses, neurons may be able to modify the activity of their neighbors. In this study we identify two genes that contribute to electrical synapses between two sensory neurons in C. elegans. We show that these electrical synapses are crucial for proper modulation of sensory responses, as without them animals are overly responsive to an aversive stimulus. In addition to pinpointing their sites of action, we present evidence that they may be contributing to neuromodulation by facilitating passage of the small molecule cGMP between neurons. Our work provides evidence for a role of electrical synapses in regulating animal behavior.


2007 ◽  
Vol 19 (3) ◽  
pp. 315-323 ◽  
Author(s):  
Ayako Watanabe ◽  
◽  
Masaki Ogino ◽  
Minoru Asada ◽  
◽  
...  

Sympathy is a key issue in interaction and communication between robots and their users. In developmental psychology, intuitive parenting is considered the maternal scaffolding upon which children develop sympathy when caregivers mimic or exaggerate the child’s emotional facial expressions [1]. We model human intuitive parenting using a robot that associates a caregiver’s mimicked or exaggerated facial expressions with the robot’s internal state to learn a sympathetic response. The internal state space and facial expressions are defined using psychological studies and change dynamically in response to external stimuli. After learning, the robot responds to the caregiver’s internal state by observing human facial expressions. The robot then expresses its own internal state facially if synchronization evokes a response to the caregiver’s internal state.


PLoS Genetics ◽  
2021 ◽  
Vol 17 (8) ◽  
pp. e1009724
Author(s):  
Di Guo ◽  
Yi-Jie Zhang ◽  
Su Zhang ◽  
Jian Li ◽  
Chao Guo ◽  
...  

Feeding is essential for animal survival and reproduction and is regulated by both internal states and external stimuli. However, little is known about how internal states influence the perception of external sensory cues that regulate feeding behavior. Here, we investigated the neuronal and molecular mechanisms behind nutritional state-mediated regulation of gustatory perception in control of feeding behavior in the brown planthopper and Drosophila. We found that feeding increases the expression of the cholecystokinin-like peptide, sulfakinin (SK), and the activity of a set of SK-expressing neurons. Starvation elevates the transcription of the sugar receptor Gr64f and SK negatively regulates the expression of Gr64f in both insects. Interestingly, we found that one of the two known SK receptors, CCKLR-17D3, is expressed by some of Gr64f-expressing neurons in the proboscis and proleg tarsi. Thus, we have identified SK as a neuropeptide signal in a neuronal circuitry that responds to food intake, and regulates feeding behavior by diminishing gustatory receptor gene expression and activity of sweet sensing GRNs. Our findings demonstrate one nutritional state-dependent pathway that modulates sweet perception and thereby feeding behavior, but our experiments cannot exclude further parallel pathways. Importantly, we show that the underlying mechanisms are conserved in the two distantly related insect species.


2021 ◽  
Author(s):  
Daniel Muench ◽  
Dennis Goldschmidt ◽  
Carlos Ribeiro

When deciding what to eat, animals evaluate sensory information about food quality alongside multiple ongoing internal states. How internal states interact to alter sensorimotor processing and shape decisions such as food choice remains poorly understood. Here, we use pan-neuronal volumetric activity imaging in the Drosophila brain to investigate the neuronal basis of internal state dependent nutrient appetites. We created a functional atlas of the ventral fly brain and find that metabolic state shapes sensorimotor processing across large sections of the neuropil. Reproductive state, in contrast, acts locally to define how sensory information is translated into feeding motor output. Thereby, these two states synergistically modulate protein-specific food intake and thus food choice. Finally, using a novel computational strategy, we identify driver lines innervating state-modulated regions and show that the newly identified borboleta region is sufficient to direct food choice towards protein-rich food. We therefore identify a generalizable principle by which distinct internal states are integrated to shape decision-making and propose a strategy to uncover and functionally validate how internal states shape behavior.


2021 ◽  
pp. 026988112110297
Author(s):  
Wayne Meighan ◽  
Thomas W Elston ◽  
David Bilkey ◽  
Ryan D Ward

Background: Animal models of psychiatric diseases suffer from a lack of reliable methods for accurate assessment of subjective internal states in nonhumans. This gap makes translation of results from animal models to patients particularly challenging. Aims/methods: Here, we used the drug-discrimination paradigm to allow rats that model a risk factor for schizophrenia (maternal immune activation, MIA) to report on the subjective internal state produced by a subanesthetic dose of the N-methyl-D-aspartate (NMDA) receptor antagonist ketamine. Results/outcomes: The MIA rats’ discrimination of ketamine was impaired relative to controls, both in the total number of rats that acquired and the asymptotic level of discrimination accuracy. This deficit was not due to a general inability to learn to discriminate an internal drug cue or internal state generally, as MIA rats were unimpaired in the learning and acquisition of a morphine drug discrimination and were as sensitive to the internal state of satiety as controls. Furthermore, the deficit was not due to a decreased sensitivity to the physiological effects of ketamine, as MIA rats showed increased ketamine-induced locomotor activity. Finally, impaired discrimination of ketamine was only seen at subanesthetic doses which functionally correspond to psychotomimetic doses in humans. Conclusion: These data link changes in NMDA responses to the MIA model. Furthermore, they confirm the utility of the drug-discrimination paradigm for future inquiries into the subjective internal state produced in models of schizophrenia and other developmental diseases.


Energies ◽  
2021 ◽  
Vol 14 (4) ◽  
pp. 969
Author(s):  
Eric Cayeux ◽  
Benoît Daireaux ◽  
Adrian Ambrus ◽  
Rodica Mihai ◽  
Liv Carlsen

The drilling process is complex because unexpected situations may occur at any time. Furthermore, the drilling system is extremely long and slender, therefore prone to vibrations and often being dominated by long transient periods. Adding the fact that measurements are not well distributed along the drilling system, with the majority of real-time measurements only available at the top side and having only access to very sparse data from downhole, the drilling process is poorly observed therefore making it difficult to use standard control methods. Therefore, to achieve completely autonomous drilling operations, it is necessary to utilize a method that is capable of estimating the internal state of the drilling system from parsimonious information while being able to make decisions that will keep the operation safe but effective. A solution enabling autonomous decision-making while drilling has been developed. It relies on an optimization of the time to reach the section total depth (TD). The estimated time to reach the section TD is decomposed into the effective time spent in conducting the drilling operation and the likely time lost to solve unexpected drilling events. This optimization problem is solved by using a Markov decision process method. Several example scenarios have been run in a virtual rig environment to test the validity of the concept. It is found that the system is capable to adapt itself to various drilling conditions, as for example being aggressive when the operation runs smoothly and the estimated uncertainty of the internal states is low, but also more cautious when the downhole drilling conditions deteriorate or when observations tend to indicate more erratic behavior, which is often observed prior to a drilling event.


2013 ◽  
Vol 110 (3) ◽  
pp. 621-639 ◽  
Author(s):  
Bryan M. Krause ◽  
Matthew I. Banks

The neural mechanisms of sensory responses recorded from the scalp or cortical surface remain controversial. Evoked vs. induced response components (i.e., changes in mean vs. variance) are associated with bottom-up vs. top-down processing, but trial-by-trial response variability can confound this interpretation. Phase reset of ongoing oscillations has also been postulated to contribute to sensory responses. In this article, we present evidence that responses under passive listening conditions are dominated by variable evoked response components. We measured the mean, variance, and phase of complex time-frequency coefficients of epidurally recorded responses to acoustic stimuli in rats. During the stimulus, changes in mean, variance, and phase tended to co-occur. After the stimulus, there was a small, low-frequency offset response in the mean and modest, prolonged desynchronization in the alpha band. Simulations showed that trial-by-trial variability in the mean can account for most of the variance and phase changes observed during the stimulus. This variability was state dependent, with smallest variability during periods of greatest arousal. Our data suggest that cortical responses to auditory stimuli reflect variable inputs to the cortical network. These analyses suggest that caution should be exercised when interpreting variance and phase changes in terms of top-down cortical processing.


Author(s):  
Giacomo Zilio ◽  
Louise Solveig Noergaard ◽  
Giovanni Petrucci ◽  
Nathalie Zeballos ◽  
Claire Gougat-Barbera ◽  
...  

Dispersal plays a main role in determining spatial dynamics, and both theory and empirical evidence indicate that evolutionary optima exist for constitutive or plastic dispersal behaviour. Plasticity in dispersal can be influenced by factors both internal (state-dependent) or external (context-dependent) to individuals. Parasitism is interesting in this context, as it can influence both types of host dispersal plasticity: individuals can disperse in response to internal infection status but might also respond to the presence of infected individuals around them. We still know little about the driving evolutionary forces of host dispersal plasticity, but a first requirement is the presence of a genetic basis on which natural selection can act. In this study, we used microcosm dispersal mazes to investigate plastic dispersal of 20 strains of the freshwater protist Paramecium caudatum in response to the bacterial parasite Holospora undulata. We additionally quantified the genetic component of the plastic responses, i.e. the heritability of state- and context-depended dispersal. We found that infection by the parasite can either increase or decrease dispersal of individual strains relative to the uninfected (state-dependent plasticity), and this to be heritable. We also found strain-specific change of dispersal of uninfected Paramecium when exposed to variable infection prevalence (context-dependent plasticity) with very low level of heritability. To our knowledge, this is the first explicit empirical demonstration and quantification of genetic variation of plastic dispersal in a host-parasite system, which could have important implications for meta-population and epidemiological dynamics. We discuss some of the underlying mechanisms of this variation and link our results to the existing theoretical models.


2020 ◽  
Vol 30 (06) ◽  
pp. 1041-1073
Author(s):  
Benoit Perthame ◽  
Weiran Sun ◽  
Min Tang ◽  
Shugo Yasuda

The run and tumble process is well established in order to describe the movement of bacteria in response to a chemical stimulus. However, the relation between the tumbling rate and the internal state of bacteria is poorly understood. This study aims at deriving macroscopic models as limits of the mesoscopic kinetic equation in different regimes. In particular, we are interested in the roles of the stiffness of the response and the adaptation time in the kinetic equation. Depending on the asymptotics chosen both the standard Keller–Segel equation and the flux-limited Keller–Segel (FLKS) equation can appear. An interesting mathematical issue arises with a new type of equilibrium equation leading to solution with singularities.


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