scholarly journals Distinct lateral inhibitory circuits drive parallel processing of sensory information in the mammalian olfactory bulb

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Matthew A Geramita ◽  
Shawn D Burton ◽  
Nathan N Urban

Splitting sensory information into parallel pathways is a common strategy in sensory systems. Yet, how circuits in these parallel pathways are composed to maintain or even enhance the encoding of specific stimulus features is poorly understood. Here, we have investigated the parallel pathways formed by mitral and tufted cells of the olfactory system in mice and characterized the emergence of feature selectivity in these cell types via distinct lateral inhibitory circuits. We find differences in activity-dependent lateral inhibition between mitral and tufted cells that likely reflect newly described differences in the activation of deep and superficial granule cells. Simulations show that these circuit-level differences allow mitral and tufted cells to best discriminate odors in separate concentration ranges, indicating that segregating information about different ranges of stimulus intensity may be an important function of these parallel sensory pathways.

2020 ◽  
Vol 123 (6) ◽  
pp. 2406-2425
Author(s):  
Tyler R. Sizemore ◽  
Laura M. Hurley ◽  
Andrew M. Dacks

The serotonergic system has been widely studied across animal taxa and different functional networks. This modulatory system is therefore well positioned to compare the consequences of neuromodulation for sensory processing across species and modalities at multiple levels of sensory organization. Serotonergic neurons that innervate sensory networks often bidirectionally exchange information with these networks but also receive input representative of motor events or motivational state. This convergence of information supports serotonin’s capacity for contextualizing sensory information according to the animal’s physiological state and external events. At the level of sensory circuitry, serotonin can have variable effects due to differential projections across specific sensory subregions, as well as differential serotonin receptor type expression within those subregions. Functionally, this infrastructure may gate or filter sensory inputs to emphasize specific stimulus features or select among different streams of information. The near-ubiquitous presence of serotonin and other neuromodulators within sensory regions, coupled with their strong effects on stimulus representation, suggests that these signaling pathways should be considered integral components of sensory systems.


Author(s):  
C.A. Greer ◽  
C.K. Kaliszewski ◽  
H.A. Cameron

Information processing within the mammalian olfactory bulb, following transduction of odor stimuli by the receptor cells of the epithelium, occurs at two distinct levels. First, in the glomerular layer dendrodendritic synapses from a subpopulation of interneurons onto projection neurons (mitral and tufted cells) modulate the influence of arriving sensory information. The second level of processing occurs within the external plexiform layer where a second population of interneurons, granule cells, form reciprocal dendrodendritic synapses with mitral and tufted cells to modulate the flow of information out of the olfactory bulb. This second population of interneurons has been of interest, in part, due to the recent recognition that subpopulations form microcircuits preferentially with either the mitral or the tufted cell projection neurons, thus supporting the notion of parallel processing pathways. As part of a continuing effort to characterize the properties of these neurons and their dendritic circuits we have been utilizing light microscopy of selectively stained neurons and both conventional and high voltage electron microscopy of selectively stained neurons to study the geometry and synaptology of the olfactory bulb granule cells.Sprague-Dawley rats, 12 - 60 days postnatal, were perfused with 1% paraformaldehyde and 1% glutaraldehyde followed by immersion in the fixative for 8-12 hrs. After washes in 0.1M phosphate buffer the tissue was passed through a conventional dehydration series, embedded in EPON and routinely stained with uranyl acetate and lead citrate following sectioning. In addition, littermates were processed for Golgi-EM. Tissue examined utilizing conventional EM (60 - 100kV) was cut at approximately 70 nm and mounted on formvar slotted grids. Tissue examined utilizing high voltage EM (800 - 1000 kV) was cut at 1 - 5 um and mounted on mesh grids prior to carbon coating. Serial sections studied with conventional EM were reconstructed and morphometrically assessed utilizing a PC based 3D reconstruction program.


2011 ◽  
Vol 105 (3) ◽  
pp. 1276-1294 ◽  
Author(s):  
Tara Deemyad ◽  
Leonard Maler ◽  
Maurice J. Chacron

Although serotonergic innervation of sensory brain areas is ubiquitous, its effects on sensory information processing remain poorly understood. We investigated these effects in pyramidal neurons within the electrosensory lateral line lobe (ELL) of weakly electric fish. Surprisingly, we found that 5-HT is present at different levels across the different ELL maps; the presence of 5-HT fibers was highest in the map that processes intraspecies communication signals. Electrophysiological recordings revealed that 5-HT increased excitability and burst firing through a decreased medium afterhyperpolarization resulting from reduced small-conductance calcium-activated (SK) currents as well as currents mediated by an M-type potassium channel. We next investigated how 5-HT alters responses to sensory input. 5-HT application decreased the rheobase current, increased the gain, and decreased first spike latency. Moreover, it reduced discriminability between different stimuli, as quantified by the mutual information rate. We hypothesized that 5-HT shifts pyramidal neurons into a burst-firing mode where bursts, when considered as events, can detect the presence of particular stimulus features. We verified this hypothesis using signal detection theory. Our results indeed show that serotonin-induced bursts of action potentials, when considered as events, could detect specific stimulus features that were distinct from those detected by isolated spikes. Moreover, we show the novel result that isolated spikes transmit more information after 5-HT application. Our results suggest a novel function for 5-HT in that it enables differential processing by action potential patterns in response to current injection.


Author(s):  
R.V.W. Dimlich ◽  
M.H. Biros

Although a previous study in this laboratory determined that Purkinje cells of the rat cerebellum did not appear to be damaged following 30 min of forebrain ischemia followed by 30 min of reperfusion, it was suggested that an increase in rough endoplasmic reticulum (RER) and/or polysomes had occurred in these cells. The primary objective of the present study was to morphometrically determine whether or not this increase had occurred. In addition, since there is substantial evidence that glial cells may be affected by ischemia earlier than other cell types, glial cells also were examined. To ascertain possible effects on other cerebellar components, granule cells and neuropil near Purkinje cells as well as neuropil in the molecular layer also were evaluated in this investigation.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.


Author(s):  
Owen Mackwood ◽  
Laura B. Naumann ◽  
Henning Sprekeler

AbstractIn sensory circuits with poor feature topography, stimulus-specific feedback inhibition necessitates carefully tuned synaptic circuitry. Recent experimental data from mouse primary visual cortex (V1) show that synapses between pyramidal neurons and parvalbumin-expressing (PV) inhibitory interneurons tend to be stronger for neurons that respond to similar stimulus features. The mechanism that underlies the formation of such excitatory-inhibitory (E/I) assemblies is unresolved. Here, we show that activity-dependent synaptic plasticity on input and output synapses of PV interneurons generates a circuit structure that is consistent with mouse V1. Using a computational model, we show that both forms of plasticity must act synergistically to form the observed E/I assemblies. Once established, these assemblies produce a stimulus-specific competition between pyramidal neurons. Our model suggests that activity-dependent plasticity can enable inhibitory circuits to actively shape cortical computations.


Author(s):  
Samantha Hughes ◽  
Tansu Celikel

From single-cell organisms to complex neural networks, all evolved to provide control solutions to generate context and goal-specific actions. Neural circuits performing sensorimotor computation to drive navigation employ inhibitory control as a gating mechanism, as they hierarchically transform (multi)sensory information into motor actions. Here, we focus on this literature to critically discuss the proposition that prominent inhibitory projections form sensorimotor circuits. After reviewing the neural circuits of navigation across various invertebrate species, we argue that with increased neural circuit complexity and the emergence of parallel computations inhibitory circuits acquire new functions. The contribution of inhibitory neurotransmission for navigation goes beyond shaping the communication that drives motor neurons, instead, include encoding of emergent sensorimotor representations. A mechanistic understanding of the neural circuits performing sensorimotor computations in invertebrates will unravel the minimum circuit requirements driving adaptive navigation.


2017 ◽  
Vol 284 (1862) ◽  
pp. 20170969 ◽  
Author(s):  
Brandon Pratt ◽  
Tanvi Deora ◽  
Thomas Mohren ◽  
Thomas Daniel

Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal.


2019 ◽  
Vol 9 (11) ◽  
pp. 315 ◽  
Author(s):  
Andrea Orlandi ◽  
Alice Mado Proverbio

It has been shown that selective attention enhances the activity in visual regions associated with stimulus processing. The left hemisphere seems to have a prominent role when non-spatial attention is directed towards specific stimulus features (e.g., color, spatial frequency). The present electrophysiological study investigated the time course and neural correlates of object-based attention, under the assumption of left-hemispheric asymmetry. Twenty-nine right-handed participants were presented with 3D graphic images representing the shapes of different object categories (wooden dummies, chairs, structures of cubes) which lacked detail. They were instructed to press a button in response to a target stimulus indicated at the beginning of each run. The perception of non-target stimuli elicited a larger anterior N2 component, which was likely associated with motor inhibition. Conversely, target selection resulted in an enhanced selection negativity (SN) response lateralized over the left occipito-temporal regions, followed by a larger centro-parietal P300 response. These potentials were interpreted as indexing attentional selection and categorization processes, respectively. The standardized weighted low-resolution electromagnetic tomography (swLORETA) source reconstruction showed the engagement of a fronto-temporo-limbic network underlying object-based visual attention. Overall, the SN scalp distribution and relative neural generators hinted at a left-hemispheric advantage for non-spatial object-based visual attention.


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