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

2020 ◽  
Author(s):  
Jian-You Lin ◽  
Narendra Mukherjee ◽  
Max J. Bernstein ◽  
Donald B. Katz

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.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jian-You Lin ◽  
Narendra Mukherjee ◽  
Max J Bernstein ◽  
Donald B Katz

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.


2022 ◽  
Author(s):  
Bradly Thomas Stone ◽  
Jian-You Lin ◽  
Abuzar Mahmood ◽  
Alden Joshua Sanford ◽  
Donald Katz

Gustatory Cortex (GC), a structure deeply involved in the making of consumption decisions, presumably performs this function by integrating information about taste, experiences, and internal states related to the animal’s health, such as illness. Here, we investigated this assertion, examining whether illness is represented in GC activity, and how this representation impacts taste responses and behavior. We recorded GC single-neuron activity and local field potentials (LFP) from healthy rats and (the same) rats made ill ( via LiCl injection). We show (consistent with the extant literature) that the onset of illness-related behaviors arises contemporaneously with alterations in spontaneous 7-12Hz LFP power at ~11 min following injection. This process was accompanied by reductions in single-neuron taste response magnitudes and discriminability, and with enhancements in palatability-relatedness – a result reflecting the collapse of responses toward a simple “good-bad” code arising in a specific subset of GC neurons. Overall, our data show that a state (illness) that profoundly reduces consumption changes basic properties of the sensory cortical response to tastes, in a manner that can easily explain illness’ impact on consumption.


2000 ◽  
Vol 83 (4) ◽  
pp. 1958-1971 ◽  
Author(s):  
Galen D. Kaufman ◽  
Michael E. Shinder ◽  
Adrian A. Perachio

Three classes of vestibular-related neurons were found in and near the prepositus and medial vestibular nuclei of alert or decerebrate gerbils, those responding to: horizontal translational motion, horizontal head rotation, or both. Their distribution ratios were 1:2:2, respectively. Many cells responsive to translational motion exhibited spatiotemporal characteristics with both response gain and phase varying as a function of the stimulus vector angle. Rotationally sensitive neurons were distributed as Type I, II, or III responses (sensitive to ipsilateral, contralateral, or both directions, respectively) in the ratios of 4:6:1. Four tested factors shaped the response dynamics of the sampled neurons: canal-otolith convergence, oculomotor-related activity, rotational Type (I or II), and the phase of the maximum response. Type I nonconvergent cells displayed increasing gains with increasing rotational stimulus frequency (0.1–2.0 Hz, 60°/s), whereas Type II neurons with convergent inputs had response gains that markedly decreased with increasing translational stimulus frequency (0.25–2.0 Hz, ±0.1 g). Type I convergent and Type II nonconvergent neurons exhibited essentially flat gains across the stimulus frequency range. Oculomotor-related activity was noted in 30% of the cells across all functional types, appearing as burst/pause discharge patterns related to the fast phase of nystagmus during head rotation. Oculomotor-related activity was correlated with enhanced dynamic range compared with the same category that had no oculomotor-related response. Finally, responses that were in-phase with head velocity during rotation exhibited greater gains with stimulus frequency increments than neurons with out-of-phase responses. In contrast, for translational motion, neurons out of phase with head acceleration exhibited low-pass characteristics, whereas in-phase neurons did not. Data from decerebrate preparations revealed that although similar response types could be detected, the sampled cells generally had lower background discharge rates, on average one-third lower response gains, and convergent properties that differed from those found in the alert animals. On the basis of the dynamic response of identified cell types, we propose a pair of models in which inhibitory input from vestibular-related neurons converges on oculomotor neurons with excitatory inputs from the vestibular nuclei. Simple signal convergence and combinations of different types of vestibular labyrinth information can enrich the dynamic characteristics of the rotational and translational vestibuloocular responses.


2020 ◽  
Author(s):  
Elor Arieli ◽  
Ron Gerbi ◽  
Mark Shein-Idelson ◽  
Anan Moran

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.


2018 ◽  
Author(s):  
Camila Demaestri ◽  
Heather C. Brenhouse ◽  
Jennifer A. Honeycutt

AbstractThe communicative role of ultrasonic vocalizations (USVs) in rodents is well established, with distinct USVs indicative of different affective states. USVs in the 22kHz range are typically emitted by adult rats when in anxiety-or fear-provoking situations (e.g. predator odor, social defeat), while 55kHz range USVs are emitted in appetitive situations (e.g., play, anticipation of reward). Previous work indicates that USVs (real-time and playback) can effectively communicate these affective states and influence changes in behavior and neural activity of the receiver. Changes in cFos activation following 22kHz USVs have been seen in cortical and limbic regions involved in anxiety, including the basolateral amygdala (BLA). However, it is unknown how USV playback influences cFos activity within the basal nucleus of the stria terminalis (BNST), a region also thought to be critical in processing anxiety-related information. The present work sought to characterize distinct behavioral, physiological, and neural responses in rats presented with aversive (22kHz) compared to appetitive (55kHz) USVs or silence. Our findings show that rats exposed to 22kHz USVs: 1) engage in anxiety-like behaviors in the open field and elevated zero maze, and 2) show distinct patterns of cFos activation within the BLA and BNST that contrast those seen in 55kHz playback. Specifically, 22kHz USVs increased cFos density in the anterodorsal nuclei, while 55kHz playback increased cFos in the oval nucleus of the BNST. These results provide important groundwork for leveraging ethologically-relevant stimuli in the rat to improve our understanding of anxiety-related responses in both typical and pathological populations.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Ethan A Heming ◽  
Kevin P Cross ◽  
Tomohiko Takei ◽  
Douglas J Cook ◽  
Stephen H Scott

Several lines of research demonstrate that primary motor cortex (M1) is principally involved in controlling the contralateral side of the body. However, M1 activity has been correlated with both contralateral and ipsilateral limb movements. Why does ipsilaterally-related activity not cause contralateral motor output? To address this question, we trained monkeys to counter mechanical loads applied to their right and left limbs. We found >50% of M1 neurons had load-related activity for both limbs. Contralateral loads evoked changes in activity ~10ms sooner than ipsilateral loads. We also found corresponding population activities were distinct, with contralateral activity residing in a subspace that was orthogonal to the ipsilateral activity. Thus, neural responses for the contralateral limb can be extracted without interference from the activity for the ipsilateral limb, and vice versa. Our results show that M1 activity unrelated to downstream motor targets can be segregated from activity related to the downstream motor output.


2021 ◽  
Author(s):  
Joshua P. Kulasingham ◽  
Neha H. Joshi ◽  
Mohsen Rezaeizadeh ◽  
Jonathan Z. Simon

AbstractCortical processing of arithmetic and of language rely on both shared and task-specific neural mechanisms, which should also be dissociable from the particular sensory modality used to probe them. Here, spoken arithmetical and non-mathematical statements were employed to investigate neural processing of arithmetic, compared to general language processing, in an attention-modulated cocktail party paradigm. Magnetoencephalography data was recorded from 22 subjects listening to both sentences and arithmetic equations while selectively attending to one of the two speech streams. Short sentences and simple equations were presented diotically at fixed and distinct word/symbol and sentence/equation rates. Critically, this allowed neural responses to acoustics, words, and symbols to be dissociated from responses to sentences and equations. Indeed, the simultaneous neural processing of the acoustics of words and symbols was observed in auditory cortex for both streams. Neural tracking of sentences and equations, however, was predominantly of the attended stream, and originated primarily from left temporal, and parietal areas, respectively. Additionally, these neural responses were correlated with behavioral performance in a deviant detection task. Source-localized Temporal Response Functions revealed cortical dynamics of distinct responses to sentences in left temporal areas and equations in bilateral temporal, parietal and motor areas. Finally, the target of attention could be decoded from responses, especially in left superior parietal areas. In short, the neural responses to arithmetic and language are especially well segregated during the cocktail party paradigm, and the correlation with behavior suggests that these neural responses are linked to successful comprehension or calculation.Significance StatementNeural processing of arithmetic relies on dedicated, modality independent cortical networks that are distinct from those underlying language processing. Using a simultaneous cocktail party listening paradigm, we found that these separate networks segregate naturally when listeners selectively attend to one type over the other. Time-locked activity in the left temporal lobe was observed for responses to both spoken sentences and equations, but the latter additionally showed bilateral parietal activity consistent with arithmetic processing. Critically, these responses were modulated by selective attention and correlated with task behavior, consistent with reflecting high-level processing for speech comprehension or correct calculations. The response dynamics show task-related differences that were used to reliably decode the attentional target of sentences or equations.


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