scholarly journals Spatial and Temporal Organization of Odor-evoked Responses in a Fly Olfactory Circuit: Inputs, Outputs and Idiosyncrasies

2020 ◽  
Author(s):  
Haoyang Rong ◽  
Lijun Zhang ◽  
Cody Greer ◽  
Yehuda Ben-Shahar ◽  
Tim Holy ◽  
...  

AbstractHow is sensory information routed through different types of neurons within a circuit, and do equivalent circuits in different individuals follow similar organizational principles? We examined this issue in the fruit fly olfactory system. Odor-evoked signals from sensory neurons (ORNs) triggered neural responses that were patterned over space and time in cholinergic ePNs and GABAergic iPNs within the antennal lobe. The dendritic-axonal (I/O) response mapping was complex and diverse, and axonal organization was region-specific (mushroom body vs. lateral horn). In the lateral horn, feed-forward excitatory and inhibitory axonal projections matched ‘odor tuning’ in a stereotyped, dorsal-lateral locus, but mismatched in most other locations. In the temporal dimension, ORN, ePN and iPN odor-evoked responses had similar encoding features, such as information refinement over time and divergent ON and OFF responses. Notably, analogous spatial and temporal coding principles were observed in all flies, and the latter emerged from idiosyncratic neural processing approaches.HighlightsConsistency and idiosyncrasy both exist in ORN, ePN and iPN functional mapsSignal transformations between different ePN compartments are complex and diverseTemporal decorrelation between stimuli happens in all three neuronal populationsOFF responses that are orthogonal to ON responses emerge after odor termination

2021 ◽  
Author(s):  
Mehdi Sicre ◽  
Julie Meffre ◽  
Frederic Ambroggi

ABSTRACTThe thalamus is a phylogenetically well-preserved structure. Known to densely contact cortical regions, its role in the transmission of sensory information to the striatal complex has been widely reconsidered in recent years. The parafascicular of the thalamus (Pf) has been implicated the orientation of attention towards salient sensory stimuli. In a stimulus-driven reward seeking task, we sought to characterize the electrophysiological activity of Pf neurons in rats. We observed a predominance of excitatory responses over inhibitory responses for all events of the task. Neurons responded more strongly to the stimulus compared to lever-pressing and collecting reward, confirming the strong involvement of the Pf in sensory information processing. The use of long sessions allowed us to compare neuronal responses to stimuli when the animal engaged in action or when it did not. We distinguished two populations of neurons responding in an opposite way: MOTIV+ neurons responded more intensively to stimuli followed by a behavioral response than those that did not. Conversely, MOTIV-neurons responded more strongly when the stimulus was ignored by the animal. In addition, MOTIV-neurons excitations appeared at a shorter latency after the stimulus than MOTIV+ neurons. Through this encoding, Pf could perform an early selection of environmental stimuli transmitted to the striatum according to motivational level.HIGHLIGHTSPf neurons respond to reward-predicting stimuli and reward-related actionsMOTIV+ Pf neurons were more active to stimuli evoking reward-seekingMOTIV- Pf neurons were more active to stimuli ignored by the animalStimuli-evoked excitations latencies were shorter in MOTIV- than MOTIV+ neurons


2020 ◽  
Author(s):  
Guillaume Bony ◽  
Arjun A Bhaskaran ◽  
Katy Le Corf ◽  
Andreas Frick

ABSTRACTThe mouse primary somatosensory cortex (S1) processes tactile sensory information and is the largest neocortex area emphasizing the importance of this sensory modality for rodent behavior. Most of our knowledge regarding information processing in S1 stems from studies of the whisker-related barrel cortex (S1–BC), yet the processing of tactile inputs from the hind-paws is poorly understood. We used in vivo whole-cell patch-clamp recordings from layer (L) 2/3 pyramidal neurons (PNs) of the S1 hind-paw (S1-HP) region of anaesthetized wild type (WT) mice to investigate their evoked sub- and supra-threshold activity, intrinsic properties, and spontaneous activity. Approximately 45% of these L2/3 PNs responded to brief contralateral HP stimulation in a subthreshold manner, ~5% fired action potentials, and ~50% of L2/3 PNs did not respond at all. The evoked subthreshold responses had long onset- (~23 ms) and peak-latencies (~61 ms). The majority (86%) of these L2/3 PNs responded to prolonged (stance-like) HP stimulation with both on- and off-responses. HP stimulation responsive L2/3 PNs had a greater intrinsic excitability compared to non-responsive ones, possibly reflecting differences in their physiological role. Similar to S1-BC, L2/3 PNs displayed up- and down-states, and low spontaneous firing rates (~0.1 Hz). Our findings support a sparse coding scheme of operation for S1–HP L2/3 PNs and highlight both differences and similarities with L2/3 PNs from other somatosensory cortex areas.KEY POINTSResponses of layer (L) 2/3 pyramidal neurons (PNs) of the primary somatosensory hind-paw cortex (S1-HP) to contralateral hind-paw stimulation reveal both differences and similarities compared to those of somatosensory neurons responding to other tactile (e.g. whiskers, forepaw, tongue) modalities.Similar to whisker-related barrel cortex (S1-BC) and forepaw cortex (S1-FP) S1-HP L2/3 PNs show a low spontaneous firing rate and a sparse action potential coding of evoked activity.In contrast to S1-BC, brief hind-paw stimulus evoked responses display a long latency in S1-HP neurons consistent with their different functional role.The great majority of L 2/3 PNs respond to prolonged hind-paw stimulation with both on- and off-responses.These results help us to better understand sensory information processing within layer 2/3 of the neocortex and the regional differences related to various tactile modalities.


Biomolecules ◽  
2021 ◽  
Vol 11 (6) ◽  
pp. 823
Author(s):  
Goran Šimić ◽  
Mladenka Tkalčić ◽  
Vana Vukić ◽  
Damir Mulc ◽  
Ena Španić ◽  
...  

Emotions arise from activations of specialized neuronal populations in several parts of the cerebral cortex, notably the anterior cingulate, insula, ventromedial prefrontal, and subcortical structures, such as the amygdala, ventral striatum, putamen, caudate nucleus, and ventral tegmental area. Feelings are conscious, emotional experiences of these activations that contribute to neuronal networks mediating thoughts, language, and behavior, thus enhancing the ability to predict, learn, and reappraise stimuli and situations in the environment based on previous experiences. Contemporary theories of emotion converge around the key role of the amygdala as the central subcortical emotional brain structure that constantly evaluates and integrates a variety of sensory information from the surroundings and assigns them appropriate values of emotional dimensions, such as valence, intensity, and approachability. The amygdala participates in the regulation of autonomic and endocrine functions, decision-making and adaptations of instinctive and motivational behaviors to changes in the environment through implicit associative learning, changes in short- and long-term synaptic plasticity, and activation of the fight-or-flight response via efferent projections from its central nucleus to cortical and subcortical structures.


2005 ◽  
Vol 94 (3) ◽  
pp. 2182-2194 ◽  
Author(s):  
Katja Karmeier ◽  
Holger G. Krapp ◽  
Martin Egelhaaf

Coding of sensory information often involves the activity of neuronal populations. We demonstrate how the accuracy of a population code depends on integration time, the size of the population, and noise correlation between the participating neurons. The population we study consists of 10 identified visual interneurons in the blowfly Calliphora vicina involved in optic flow processing. These neurons are assumed to encode the animal's head or body rotations around horizontal axes by means of graded potential changes. From electrophysiological experiments we obtain parameters for modeling the neurons' responses. From applying a Bayesian analysis on the modeled population response we draw three major conclusions. First, integration of neuronal activities over a time period of only 5 ms after response onset is sufficient to decode accurately the rotation axis. Second, noise correlation between neurons has only little impact on the population's performance. And third, although a population of only two neurons would be sufficient to encode any horizontal rotation axis, the population of 10 vertical system neurons is advantageous if the available integration time is short. For the fly, short integration times to decode neuronal responses are important when controlling rapid flight maneuvers.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Javier Jimenez-Martin ◽  
Daniil Potapov ◽  
Kay Potapov ◽  
Thomas Knöpfel ◽  
Ruth M. Empson

AbstractCholinergic modulation of brain activity is fundamental for awareness and conscious sensorimotor behaviours, but deciphering the timing and significance of acetylcholine actions for these behaviours is challenging. The widespread nature of cholinergic projections to the cortex means that new insights require access to specific neuronal populations, and on a time-scale that matches behaviourally relevant cholinergic actions. Here, we use fast, voltage imaging of L2/3 cortical pyramidal neurons exclusively expressing the genetically-encoded voltage indicator Butterfly 1.2, in awake, head-fixed mice, receiving sensory stimulation, whilst manipulating the cholinergic system. Altering muscarinic acetylcholine function re-shaped sensory-evoked fast depolarisation and subsequent slow hyperpolarisation of L2/3 pyramidal neurons. A consequence of this re-shaping was disrupted adaptation of the sensory-evoked responses, suggesting a critical role for acetylcholine during sensory discrimination behaviour. Our findings provide new insights into how the cortex processes sensory information and how loss of acetylcholine, for example in Alzheimer’s Disease, disrupts sensory behaviours.


1991 ◽  
Vol 3 (2) ◽  
pp. 155-166 ◽  
Author(s):  
Peter König ◽  
Thomas B. Schillen

Current concepts in neurobiology of vision assume that local object features are represented by distributed neuronal populations in the brain. Such representations can lead to ambiguities if several distinct objects are simultaneously present in the visual field. Temporal characteristics of the neuronal activity have been proposed as a possible solution to this problem and have been found in various cortical areas. In this paper we introduce a delayed nonlinear oscillator to investigate temporal coding in neuronal networks. We show synchronization within two-dimensional layers consisting of oscillatory elements coupled by excitatory delay connections. The observed correlation length is large compared to coupling length. Following the experimental situation, we then demonstrate the response of such layers to two short stimulus bars of varying gap distance. Coherency of stimuli is reflected by the temporal correlation of the responses, which closely resembles the experimental observations.


2013 ◽  
Vol 25 (12) ◽  
pp. 3263-3293 ◽  
Author(s):  
Samuel A. Neymotin ◽  
George L. Chadderdon ◽  
Cliff C. Kerr ◽  
Joseph T. Francis ◽  
William W. Lytton

Neocortical mechanisms of learning sensorimotor control involve a complex series of interactions at multiple levels, from synaptic mechanisms to cellular dynamics to network connectomics. We developed a model of sensory and motor neocortex consisting of 704 spiking model neurons. Sensory and motor populations included excitatory cells and two types of interneurons. Neurons were interconnected with AMPA/NMDA and GABAA synapses. We trained our model using spike-timing-dependent reinforcement learning to control a two-joint virtual arm to reach to a fixed target. For each of 125 trained networks, we used 200 training sessions, each involving 15 s reaches to the target from 16 starting positions. Learning altered network dynamics, with enhancements to neuronal synchrony and behaviorally relevant information flow between neurons. After learning, networks demonstrated retention of behaviorally relevant memories by using proprioceptive information to perform reach-to-target from multiple starting positions. Networks dynamically controlled which joint rotations to use to reach a target, depending on current arm position. Learning-dependent network reorganization was evident in both sensory and motor populations: learned synaptic weights showed target-specific patterning optimized for particular reach movements. Our model embodies an integrative hypothesis of sensorimotor cortical learning that could be used to interpret future electrophysiological data recorded in vivo from sensorimotor learning experiments. We used our model to make the following predictions: learning enhances synchrony in neuronal populations and behaviorally relevant information flow across neuronal populations, enhanced sensory processing aids task-relevant motor performance and the relative ease of a particular movement in vivo depends on the amount of sensory information required to complete the movement.


2021 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
Andre Fiala ◽  
Gaia Tavosanis

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.


Author(s):  
Arne F. Meyer ◽  
John O’Keefe ◽  
Jasper Poort

SummaryAnimals actively interact with their environment to gather sensory information. There is conflicting evidence about how mice use vision to sample their environment. During head restraint, mice make rapid eye movements strongly coupled between the eyes, similar to conjugate saccadic eye movements in humans. However, when mice are free to move their heads, eye movement patterns are more complex and often non-conjugate, with the eyes moving in opposite directions. Here, we combined eye tracking with head motion measurements in freely moving mice and found that both observations can be explained by the existence of two distinct types of coupling between eye and head movements. The first type comprised non-conjugate eye movements which systematically compensated for changes in head tilt to maintain approximately the same visual field relative to the horizontal ground plane. The second type of eye movements were conjugate and coupled to head yaw rotation to produce a “saccade and fixate” gaze pattern. During head initiated saccades, the eyes moved together in the same direction as the head, but during subsequent fixation moved in the opposite direction to the head to compensate for head rotation. This “saccade and fixate” pattern is similar to that seen in humans who use eye movements (with or without head movement) to rapidly shift gaze but in mice relies on combined eye and head movements. Indeed, the two types of eye movements very rarely occurred in the absence of head movements. Even in head-restrained mice, eye movements were invariably associated with attempted head motion. Both types of eye-head coupling were seen in freely moving mice during social interactions and a visually-guided object tracking task. Our results reveal that mice use a combination of head and eye movements to sample their environment and highlight the similarities and differences between eye movements in mice and humans.HighlightsTracking of eyes and head in freely moving mice reveals two types of eye-head couplingEye/head tilt coupling aligns gaze to horizontal planeRotational eye and head coupling produces a “saccade and fixate” gaze pattern with head leading the eyeBoth types of eye-head coupling are maintained during visually-guided behaviorsEye movements in head-restrained mice are related to attempted head movements


2017 ◽  
Author(s):  
Haoyang Rong ◽  
Prithwiraj Das ◽  
Adalee Lube ◽  
David Yang ◽  
Debajit Saha ◽  
...  

HighlightsA novel geotaxis assay showed high intensity odorant exposures are harmful to fliesRepulsion at high odor intensities can be a protective mechanismOlfactory receptor neuron (ORN) excitability abruptly changes with odor intensityA linear combination of ORN activities can robustly predict intensity-dependent behavioral repulsionSummaryThe olfactory system is uniquely positioned to warn an organism of environmental threats. Whether and how it encodes such information is not understood. Here, we examined this issue in the fruit fly Drosophila melanogaster. We found that intensity-dependent repulsion to chemicals safeguarded flies from harmful, high-intensity vapor exposures. To understand how sensory input changed as the odor valence switched from innocuous to threatening, we recorded from olfactory receptor neurons (ORNs) in the fly antenna. Primarily, we observed two response non-linearities: recruitment of non-active ORNs at higher intensities, and abrupt transitions in neural excitability from regular spiking to high-firing oscillatory regime. Although non-linearities observed in any single ORN was not a good indicator, a simple linear combination of firing events from multiple neurons provided robust recognition of threating/repulsive olfactory stimuli. In sum, our results reveal how information necessary to avoid environmental threats may also be encoded in the insect antenna.


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