scholarly journals Dynamic inhibition of sensory responses mediated by an olfactory corticofugal system

2020 ◽  
Author(s):  
Renata Medinaceli Quintela ◽  
Jennifer Bauer ◽  
Lutz Wallhorn ◽  
Daniela Brunert ◽  
Markus Rothermel
Keyword(s):  
Olfactory Bulb ◽  
Sensory Information ◽  
Olfactory Cortex ◽  
Sensory Response ◽  
Anterior Olfactory Nucleus ◽  
Output Neurons ◽  
Olfactory Processing ◽  
Tufted Cells ◽  
Sensory Responses ◽  
Sensory Evoked

AbstractProcessing of sensory information is substantially modulated by centrifugal projections from higher cortical areas, yet their behavioral relevance and underlying neural mechanisms remain unclear in most cases. The anterior olfactory nucleus (AON) is part of the olfactory cortex and its extensive connections to lower and higher brain centers put it in a prime position to modulate early sensory information in the olfactory system. Here, we show that optogenetic activation of AON neurons in awake animals was not perceived as an odorant equivalent cue. However, AON activation during odorant presentation reliably suppressed odor responses. This AON mediated effect was fast and constant across odors and concentrations. Likewise, activation of glutamatergic AON projections to the olfactory bulb (OB) transiently inhibited the excitability of mitral/tufted cells (MTCs) that relay olfactory input to cortex. Single-unit MTC recordings revealed that optogenetic activation of glutamatergic AON terminals in the OB transiently decreased sensory-evoked MTC spiking, regardless of the strength or polarity of the sensory response. These findings suggest that glutamatergic AON projections to the OB suppress early olfactory processing by inhibiting OB output neurons and that the AON can dynamically gate sensory throughput to the cortex.Significance StatementThe anterior olfactory nucleus (AON) as an olfactory information processing area sends extensive projections to lower and higher brain centers but the behavioral consequences of its activation have been scarcely investigated. Using behavioral tests in combination with optogenetic manipulation we show that in contrast to what has been suggested previously, the AON does not seem to form odor percepts but instead suppresses odor responses across odorants and concentrations. Furthermore, this study shows that glutamatergic cortical projections to the olfactory bulb suppress olfactory processing by inhibiting output neurons, pointing to a potential mechanisms by which the olfactory cortex can actively and dynamically gate sensory throughput to higher brain centers.HighlightsAON stimulation suppresses odor responses across odorants and concentrationsAON activation is not perceived as an odorant equivalent cueThe AON dynamically shapes olfactory bulb output on a fast timescaleAON input to the olfactory bulb strongly suppresses mitral/tufted cells firing

Olfactory Circuitry and Behavioral Decisions

2020 ◽  
Vol 83 (1) ◽  
Author(s):  
Kensaku Mori ◽  
Hitoshi Sakano
Keyword(s):  
Olfactory Bulb ◽  
Behavioral Responses ◽  
Olfactory Cortex ◽  
Annual Review ◽  
Publication Date ◽  
Mitral Cells ◽  
Topographic Map ◽  
Input Signals ◽  
Tufted Cells ◽  
Odor Signals

In mammals, odor information detected by olfactory sensory neurons is converted to a topographic map of activated glomeruli in the olfactory bulb. Mitral cells and tufted cells transmit signals sequentially to the olfactory cortex for behavioral outputs. To elicit innate behavioral responses, odor signals are directly transmitted by distinct subsets of mitral cells from particular functional domains in the olfactory bulb to specific amygdala nuclei. As for the learned decisions, input signals are conveyed by tufted cells as well as by mitral cells to the olfactory cortex. Behavioral scene cells link the odor information to the valence cells in the amygdala to elicit memory-based behavioral responses. Olfactory decision and perception take place in relation to the respiratory cycle. How is the sensory quality imposed on the olfactory inputs for behavioral outputs? How are the two types of odor signals, innate and learned, processed during respiration? Here, we review recent progress on the study of neural circuits involved in decision making in the mouse olfactory system. Expected final online publication date for the Annual Review of Physiology, Volume 83 is February 10, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Role of intraglomerular circuits in shaping temporally structured responses to naturalistic inhalation-driven sensory input to the olfactory bulb

2015 ◽  
Vol 113 (9) ◽  
pp. 3112-3129 ◽  
Author(s):  
Ryan M. Carey ◽  
William Erik Sherwood ◽  
Michael T. Shipley ◽  
Alla Borisyuk ◽  
Matt Wachowiak
Keyword(s):  
Olfactory Bulb ◽  
Sensory Neuron ◽  
Temporal Structure ◽  
Decay Kinetics ◽  
Response Dynamics ◽  
Output Neurons ◽  
Tufted Cells ◽  
Slow Onset ◽  
Feedforward Inhibition

Olfaction in mammals is a dynamic process driven by the inhalation of air through the nasal cavity. Inhalation determines the temporal structure of sensory neuron responses and shapes the neural dynamics underlying central olfactory processing. Inhalation-linked bursts of activity among olfactory bulb (OB) output neurons [mitral/tufted cells (MCs)] are temporally transformed relative to those of sensory neurons. We investigated how OB circuits shape inhalation-driven dynamics in MCs using a modeling approach that was highly constrained by experimental results. First, we constructed models of canonical OB circuits that included mono- and disynaptic feedforward excitation, recurrent inhibition and feedforward inhibition of the MC. We then used experimental data to drive inputs to the models and to tune parameters; inputs were derived from sensory neuron responses during natural odorant sampling (sniffing) in awake rats, and model output was compared with recordings of MC responses to odorants sampled with the same sniff waveforms. This approach allowed us to identify OB circuit features underlying the temporal transformation of sensory inputs into inhalation-linked patterns of MC spike output. We found that realistic input-output transformations can be achieved independently by multiple circuits, including feedforward inhibition with slow onset and decay kinetics and parallel feedforward MC excitation mediated by external tufted cells. We also found that recurrent and feedforward inhibition had differential impacts on MC firing rates and on inhalation-linked response dynamics. These results highlight the importance of investigating neural circuits in a naturalistic context and provide a framework for further explorations of signal processing by OB networks.

Time-Dependent, Layer-Specific Modulation of Sensory Responses Mediated by Neocortical Layer 1

2006 ◽  
Vol 96 (6) ◽  
pp. 3170-3182 ◽  
Author(s):  
Dan Shlosberg ◽  
Yael Amitai ◽  
Rony Azouz
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Sensory Information ◽  
Time Dependent ◽  
Inhibitory Influence ◽  
Sensory Responses ◽  
Specific Regulation ◽  
Sensory Evoked

An essential component of feedback and top-down information in the cortical column arrives at layer 1 (L1) where it contacts distal dendrites of pyramidal neurons. Although much is known about the anatomical organization of L1 fibers, their contribution to sensory information processing remains to be determined. We assessed the physiological significance of L1 inputs by performing extracellular recordings in vivo from neurons in the primary somatosensory cortex of rodents. We found that blocking activity in L1 increases whisker-evoked response magnitude and variance, suggesting that L1 exerts an inhibitory influence on whisker responses. However, when pairing L1 stimulation with whisker deflection, the interval between the stimuli determined the outcome of the interaction, with facilitation of sensory responses dominating the short intervals (≤10 ms) and suppression prevailing at longer intervals (>10 ms). These temporal interactions resulted in a time-dependent regulation of direction tuning of cortical neurons. The synaptic mechanisms underlying L1 inputs’ influences were examined using whole cell recordings in vitro while pairing L1 and white-matter stimulations. We found time-dependent, layer-specific differences in synaptic summation of the two inputs, with supralinearity at shorter intervals and sublinearity at longer intervals that resulted mainly from shunting inhibition. Taken together, our results demonstrate that L1 inputs impose a time- and layer-specific regulation on sensory-evoked responses. This in turn may lead to a dynamic transmission of sensory information in the somatosensory cortex.

scholarly journals Spontaneous activity generated within the olfactory bulb establishes the discrete wiring of mitral cell dendrites

2019 ◽  
Author(s):  
Satoshi Fujimoto ◽  
Marcus N. Leiwe ◽  
Richi Sakaguchi ◽  
Yuko Muroyama ◽  
Reiko Kobayakawa ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Spontaneous Activity ◽  
Neuronal Activity ◽  
Primary Dendrite ◽  
Sensory Information ◽  
Mitral Cell ◽  
Network Activity ◽  
Mitral Cells ◽  
Tufted Cells

ABSTRACTIn the mouse olfactory bulb, sensory information detected by ∼1,000 types of olfactory sensory neurons (OSNs) is represented by the glomerular map. The second-order neurons, mitral and tufted cells, connect a single primary dendrite to one glomerulus. This forms discrete connectivity between the ∼1,000 types of input and output neurons. It has remained unknown how this discrete dendrite wiring is established during development. We found that genetically silencing neuronal activity in mitral cells, but not from OSNs, perturbs the dendrite pruning of mitral cells. In vivo calcium imaging of awake neonatal animals revealed two types of spontaneous neuronal activity in mitral/tufted cells, but not in OSNs. Pharmacological and knockout experiments revealed a role for glutamate and NMDARs. The genetic blockade of neurotransmission among mitral/tufted cells reduced spontaneous activity and perturbed dendrite wiring. Thus, spontaneous network activity generated within the olfactory bulb self-organizes the parallel discrete connections in the mouse olfactory system.

scholarly journals Temporal dynamics of inhalation-linked activity across defined subpopulations of mouse olfactory bulb neurons imaged in vivo

2019 ◽  
Author(s):  
Shaina M. Short ◽  
Matt Wachowiak
Keyword(s):  
Olfactory Bulb ◽  
Temporal Dynamics ◽  
Cell Types ◽  
Response Patterns ◽  
Two Photon ◽  
Cell Type Specific ◽  
Olfactory Processing ◽  
Tufted Cells ◽  
Cell Subpopulations

ABSTRACTIn mammalian olfaction, inhalation drives the temporal patterning of neural activity that underlies early olfactory processing, and a single inhalation of odorant is sufficient for odor perception. However, how the neural circuits that process incoming olfactory information are activated in the context of inhalation-linked dynamics remains poorly understood. To better understand early olfactory processing in vivo, we used an artificial inhalation paradigm combined with two-photon calcium imaging to compare the dynamics of activity evoked by odorant inhalation across major cell types of the mouse olfactory bulb. Transgenic models and cell-type specific genetic tools were used to express GCaMP6f or jRGECO1a in mitral and tufted cell subpopulations, olfactory sensory neurons and two major juxtaglomerular interneuron classes, and responses to a single inhalation of odorant were compared. Activity in all cell types was strongly linked to inhalation, and all cell types showed some variance in the latency, rise-times and durations of their inhalation-linked response patterns. The dynamics of juxtaglomerular interneuron activity closely matched that of sensory neuron inputs, while mitral and tufted cells showed the highest diversity in dynamics, with a range of latencies and durations that could not be accounted for by heterogeneity in the dynamics of sensory input. Surprisingly, temporal response patterns of mitral and superficial tufted cells were highly overlapping such that these two subpopulations could not be distinguished on the basis of their inhalation-linked dynamics, with the exception of a subpopulation of superficial tufted cells expressing the peptide transmitter cholecystokinin. Overall, these results support a model in which diversity in inhalation-linked patterning of OB output arises first at the level of OSN inputs to the OB and is enhanced by feedforward inhibition from juxtaglomerular interneurons which differentially impacts different subpopulations of OB output neurons.

scholarly journals Long-range GABAergic inhibition modulates spatiotemporal dynamics of the output neurons in the olfactory bulb

2020 ◽  
Author(s):  
Pablo S. Villar ◽  
Ruilong Hu ◽  
Ricardo C. Araneda
Keyword(s):  
Olfactory Bulb ◽  
Long Range ◽  
Granule Cells ◽  
Brain Slices ◽  
Gabaergic Neurons ◽  
Gabaergic Inhibition ◽  
Top Down ◽  
Local Interneurons ◽  
Output Neurons ◽  
Tufted Cells

SUMMARYLocal interneurons of the olfactory bulb (OB) are densely innervated by long-range GABAergic neurons from the basal forebrain (BF), suggesting that this top-down inhibition regulates early processing in the olfactory system. However, how GABAergic inputs modulate the OB output neurons, the mitral/tufted cells, is unknown. Here, in acute brain slices, we show that optogenetic activation of BF GABAergic inputs produced distinct local circuit effects that can influence the activity of mitral/tufted cells in the spatiotemporal domains. Activation of the GABAergic axons produced a fast disinhibition of mitral/tufted cells consistent with a rapid and synchronous release of GABA onto local interneurons in the glomerular and inframitral circuits of the OB, which also reduced the spike precision of mitral/tufted cells in response to simulated stimuli. In addition, BF GABAergic inhibition modulated local oscillations in a layer-specific manner. The intensity of locally evoked θ oscillations was decreased upon activation of top-down inhibition in the glomerular circuit, while evoked γ oscillations were reduced by inhibition of granule cells. Furthermore, BF GABAergic input reduced dendrodendritic inhibition in mitral/tufted cells. Together, these results suggest that long-range GABAergic neurons from the BF are well suited to influence temporal and spatial aspects of processing by OB circuits.

scholarly journals Tuning of ventral tenia tecta neurons of the olfactory cortex to distinct scenes of feeding behavior

2018 ◽  
Author(s):  
Kazuki Shiotani ◽  
Hiroyuki Manabe ◽  
Yuta Tanisumi ◽  
Koshi Murata ◽  
Junya Hirokawa ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Olfactory Bulb ◽  
Drinking Behavior ◽  
Piriform Cortex ◽  
Sensory Information ◽  
Afferent Input ◽  
Olfactory Cortex ◽  
Top Down ◽  
Behavioral Correlates ◽  
Drinking Behaviors

AbstractVentral tenia tecta (vTT) is a part of the olfactory cortex that receives both olfactory sensory signals from the olfactory bulb and top-down signals from the prefrontal cortex. To address the question whether and how the neuronal activity of the vTT is modulated by prefrontal cognitive processes such as attention, expectation and working memory that occurs during goal-directed behaviors, we recorded individual neuronal responses in the vTT of freely moving awake mice that performed learned odor-guided feeding and drinking behaviors. We found that the firing pattern of individual vTT cells had repeatable behavioral correlates such that the environmental and behavioral scene the mouse encountered during the learned behavior was the major determinant of when individual vTT neurons fired maximally. Furthermore, spiking activity of these scene cells was modulated not only by the present scene but also by the future scene that the mouse predicted. We show that vTT receives afferent input from the olfactory bulb and top-down inputs from the medial prefrontal cortex and piriform cortex.These results indicate that different groups of vTT cells are activated at different scenes and suggest that processing of olfactory sensory information is handled by different scene cells during distinct scenes of learned feeding and drinking behaviors. In other words, during the feeding and drinking behavior, vTT changes its working mode moment by moment in accord with the scene change by selectively biasing specific scene cells. The scene effect on olfactory sensory processing in the vTT has implications for the neuronal circuit mechanisms of top-down attention and scene-dependent encoding and recall of olfactory memory.

Ultrastructural analyses of local circuits in the olfactory system

1989 ◽  
Vol 47 ◽  
pp. 790-791
Author(s):  
C.A. Greer ◽  
C.K. Kaliszewski ◽  
H.A. Cameron
Keyword(s):  
Olfactory Bulb ◽  
High Voltage ◽  
Granule Cells ◽  
Sensory Information ◽  
Projection Neurons ◽  
Sprague Dawley ◽  
High Voltage Electron Microscopy ◽  
Tufted Cells ◽  
Local Circuits ◽  
Dendrodendritic Synapses

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.

scholarly journals Differential serotonergic modulation of principal neurons and interneurons in the anterior piriform cortex

2022 ◽  
Author(s):  
Magor L Lőrincz ◽  
Ildikó Piszár
Keyword(s):  
Piriform Cortex ◽  
Sensory Information ◽  
Olfactory Cortex ◽  
Anterior Piriform Cortex ◽  
Electrophysiological Recordings ◽  
Primary Olfactory Cortex ◽  
Brainstem Raphe ◽  
Evoked Activity ◽  
Sensory Evoked

Originating from the brainstem raphe nuclei, serotonin is an important neuromodulator involved in a variety of physiological and pathological functions. Specific optogenetic stimulation of serotonergic neurons results in the divisive suppression of spontaneous, but not sensory evoked activity in the majority of neurons in the primary olfactory cortex and an increase in firing in a minority of neurons. To reveal the mechanisms involved in this dual serotonergic control of cortical activity we used a combination of in vitro electrophysiological recordings from identified neurons in the primary olfactory cortex, optogenetics and pharmacology and found that serotonin suppressed the activity of principal neurons, but excited local interneurons. The results have important implications in sensory information processing and other functions of the olfactory cortex and related brain areas.

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