scholarly journals Top-down inputs drive neuronal network rewiring and context-enhanced sensory processing in olfaction

2018 ◽  
Author(s):  
Wayne Adams ◽  
James N. Graham ◽  
Xuchen Han ◽  
Hermann Riecke
Keyword(s):  
Information Processing ◽  
Olfactory Bulb ◽  
Sensory Processing ◽  
Olfactory System ◽  
Sensory Input ◽  
Granule Cells ◽  
Top Down ◽  
Brain Areas ◽  
Bottom Up ◽  
Cluttered Environments

AbstractMuch of the computational power of the mammalian brain arises from its extensive top-down projections. To enable neuron-specific information processing these projections have to be precisely targeted. How such a specific connectivity emerges and what functions it supports is still poorly understood. We addressed these questions in silico in the context of the profound structural plasticity of the olfactory system. At the core of this plasticity are the granule cells of the olfactory bulb, which integrate bottom-up sensory inputs and top-down inputs delivered by vast top-down projections from cortical and other brain areas. We developed a biophysically supported computational model for the rewiring of the top-down projections and the intra-bulbar network via adult neurogenesis. The model captures various previous physiological and behavioral observations and makes specific predictions for the cortico-bulbar network connectivity that is learned by odor exposure and environmental contexts. Specifically, it predicts that after learning the granule-cell receptive fields with respect to sensory and with respect to cortical inputs are highly correlated. This enables cortical cells that respond to a learned odor to enact disynaptic inhibitory control specifically of bulbar principal cells that respond to that odor. Functionally, the model predicts context-enhanced stimulus discrimination in cluttered environments (‘olfactory cocktail parties’) and the ability of the system to adapt to its tasks by rapidly switching between different odor-processing modes. These predictions are experimentally testable. At the same time they provide guidance for future experiments aimed at unraveling the cortico-bulbar connectivity.Author summaryIn mammalian sensory processing, extensive top-down feedback from higher brain areas reshapes the feedforward, bottom-up information processing. The structure of the top-down connectivity, the mechanisms leading to its specificity, and the functions it supports are still poorly understood. Using computational modeling, we investigated these issues in the olfactory system. There, the granule cells of the olfactory bulb, which is the first brain area to receive sensory input from the nose, are the key players of extensive structural changes to the network through the addition and also the removal of granule cells as well as through the formation and removal of their connections. This structural plasticity allows the system to learn and to adapt its sensory processing to its odor environment. Crucially, the granule cells combine bottom-up sensory input from the nose with top-down input from higher brain areas, including cortex. Our biophysically supported computational model predicts that, after learning, the granule cells enable cortical neurons that respond to a learned odor to gain inhibitory control of principal neurons of the olfactory bulb, specifically of those that respond to the learned odor. Functionally, this allows top-down input to enhance odor discrimination in cluttered environments and to quickly switch between odor tasks.

scholarly journals Top-down feedback enables flexible coding strategies in olfactory cortex

2021 ◽  
Author(s):  
Zhen Chen ◽  
Krishnan Padmanabhan
Keyword(s):  
Olfactory Bulb ◽  
Neural Activity ◽  
Olfactory System ◽  
Granule Cells ◽  
Temporal Structure ◽  
Time Windows ◽  
Olfactory Cortex ◽  
Top Down ◽  
Cortical Cells ◽  
Detailed Model

In chemical sensation, multiple models have been proposed to explain how odors are represented by patterns of neuronal activity in the olfactory cortex. One hypothesis is that the identity of combinations of active neurons within specific sniff-related time windows are critical for encoding information about odors. Another model is that patterns of neural activity evolve across time and it is this temporal structure that is essential for encoding odor information. Interestingly, we found that top-down feedback to the olfactory bulb dictates what information is transmitted to the olfactory cortex by switching between these two strategies. Using a detailed model of the early olfactory system, we demonstrate that feedback control of inhibitory granule cells in the main olfactory bulb influences the balance between excitatory and inhibitory synaptic currents in mitral cells, thereby restructuring the firing patterns of piriform cortical cells across time. This resulted in performance gains in both the accuracy and reaction time of odor discrimination tasks. These findings lead us to propose a new framework for early olfactory computation, one in which top-down feedback to the bulb flexibly controls the temporal structure of neural activity in olfactory cortex, allowing the early olfactory system to dynamically switch between two distinct models of coding.  

scholarly journals Signature patterns for top-down and bottom-up information processing via cross-frequency coupling in macaque auditory cortex

2018 ◽  
Author(s):  
Christian D. Márton ◽  
Makoto Fukushima ◽  
Corrie R. Camalier ◽  
Simon R. Schultz ◽  
Bruno B. Averbeck
Keyword(s):  
Information Processing ◽  
Auditory Cortex ◽  
Predictive Coding ◽  
Low Frequency ◽  
Information Need ◽  
Top Down ◽  
Bottom Up ◽  
Low Frequencies ◽  
Frequency Coupling ◽  
Cross Frequency Coupling

AbstractPredictive coding is a theoretical framework that provides a functional interpretation of top-down and bottom up interactions in sensory processing. The theory has suggested that specific frequency bands relay bottom-up and top-down information (e.g. “γ up, β down”). But it remains unclear whether this notion generalizes to cross-frequency interactions. Furthermore, most of the evidence so far comes from visual pathways. Here we examined cross-frequency coupling across four sectors of the auditory hierarchy in the macaque. We computed two measures of cross-frequency coupling, phase-amplitude coupling (PAC) and amplitude-amplitude coupling (AAC). Our findings revealed distinct patterns for bottom-up and top-down information processing among cross-frequency interactions. Both top-down and bottom-up made prominent use of low frequencies: low-to-low frequency (θ, α, β) and low frequency-to-high γ couplings were predominant top-down, while low frequency-to-low γ couplings were predominant bottom-up. These patterns were largely preserved across coupling types (PAC and AAC) and across stimulus types (natural and synthetic auditory stimuli), suggesting they are a general feature of information processing in auditory cortex. Moreover, our findings showed that low-frequency PAC alternated between predominantly top-down or bottom-up over time. Altogether, this suggests sensory information need not be propagated along separate frequencies upwards and downwards. Rather, information can be unmixed by having low frequencies couple to distinct frequency ranges in the target region, and by alternating top-down and bottom-up processing over time.1SignificanceThe brain consists of highly interconnected cortical areas, yet the patterns in directional cortical communication are not fully understood, in particular with regards to interactions between different signal components across frequencies. We employed a a unified, computationally advantageous Granger-causal framework to examine bi-directional cross-frequency interactions across four sectors of the auditory cortical hierarchy in macaques. Our findings extend the view of cross-frequency interactions in auditory cortex, suggesting they also play a prominent role in top-down processing. Our findings also suggest information need not be propagated along separate channels up and down the cortical hierarchy, with important implications for theories of information processing in the brain such as predictive coding.

Multi-scale predictions distinctively modulate tone perception in schizophrenia patients with auditory verbal hallucinations

2020 ◽  
Author(s):  
Fuyin Yang ◽  
Hao Zhu ◽  
Lingfang Yu ◽  
Weihong Lu ◽  
Chen Zhang ◽  
...  
Keyword(s):  
Sensory Processing ◽  
Source Monitoring ◽  
Weighting Function ◽  
Sensitivity Index ◽  
Healthy Controls ◽  
Top Down ◽  
Bottom Up ◽  
Multiple Timescales ◽  
Temporal Characteristics ◽  
Auditory Verbal Hallucinations

AbstractsAuditory verbal hallucinations (AVHs) are one of the most pronounced symptoms that manifest the underlying mechanisms of deficits in schizophrenia. Cognitive models postulate that malfunctioned source monitoring incorrectly weights the top-down prediction and bottom-up sensory processing and causes hallucinations. Here, we investigate the featural-temporal characteristics of source monitoring in AVHs. Schizophrenia patients with and without AVHs, and healthy controls identified target tones in noise at the end of tone sequences. Predictions of different timescales were manipulated by either an alternating pattern in the preceding tone sequences, or a repetition between the target tone and the tone immediately before. The sensitivity index, d’, was obtained to assess the modulation of predictions on tone identification. We found that patients with AVHs showed higher d’ when the target tones conformed to the long-term regularity of alternating pattern in the preceding tone sequence than that when the targets were inconsistent with the pattern. Whereas, the short-term regularity of repetitions modulated the tone identification in patients without AVHs. Predictions did not influence tone identification in healthy controls. These findings suggest that malfunctioned source monitoring in AVHs heavily weights predictions to form incorrect perception. The weighting function in source monitoring can extend to the process of basic tonal features, and predictions at multiple timescales differentially modulate perception in different clinical populations. These collaboratively reveal the featural and temporal characteristics of weighting function in source monitoring of AVHs and suggest that the malfunctioned interaction between top-down and bottom-up processes might underlie the development of auditory hallucinations.HighlightsMalfunctioned source monitoring incorrectly weights the top-down prediction and bottom-up sensory processing underlie pathogenesis of auditory verbal hallucinations in schizophrenia.The weighting function in top-down predictions and bottom-up sensory processing can extend to tonal features.Predictions at multiple timescales differentially modulate perception in different clinical schizophrenia populations.

scholarly journals PACAP modulation of calcium ion activity in developing granule cells of the neonatal mouse olfactory bulb

2015 ◽  
Vol 113 (4) ◽  
pp. 1234-1248 ◽  
Author(s):  
Mavis Irwin ◽  
Ann Greig ◽  
Petr Tvrdik ◽  
Mary T. Lucero
Keyword(s):  
Olfactory Bulb ◽  
Indirect Effects ◽  
Calcium Ion ◽  
Gaba Receptors ◽  
Sensory Input ◽  
Granule Cells ◽  
Gaba Release ◽  
Network Activity ◽  
Pituitary Adenylate Cyclase ◽  
Ion Activity

Ca2+ activity in the CNS is critical for the establishment of developing neuronal circuitry prior to and during early sensory input. In developing olfactory bulb (OB), the neuromodulators that enhance network activity are largely unknown. Here we provide evidence that pituitary adenylate cyclase-activating peptide (PACAP)-specific PAC1 receptors (PAC1Rs) expressed in postnatal day (P)2–P5 mouse OB are functional and enhance network activity as measured by increases in calcium in genetically identified granule cells (GCs). We used confocal Ca2+ imaging of OB slices from Dlx2-tdTomato mice to visualize GABAergic GCs. To address whether the PACAP-induced Ca2+ oscillations were direct or indirect effects of PAC1R activation, we used antagonists for the GABA receptors (GABARs) and/or glutamate receptors (GluRs) in the presence and absence of PACAP. Combined block of GABARs and GluRs yielded a 66% decrease in the numbers of PACAP-responsive cells, suggesting that 34% of OB neurons are directly activated by PACAP. Similarly, immunocytochemistry using anti-PAC1 antibody showed that 34% of OB neurons express PAC1R. Blocking either GluRs or GABARs alone indirectly showed that PACAP stimulates release of both glutamate and GABA, which activate GCs. The appearance of PACAP-induced Ca2+ activity in immature GCs suggests a role for PACAP in GC maturation. To conclude, we find that PACAP has both direct and indirect effects on neonatal OB GABAergic cells and may enhance network activity by promoting glutamate and GABA release. Furthermore, the numbers of PACAP-responsive GCs significantly increased between P2 and P5, suggesting that PACAP-induced Ca2+ activity contributes to neonatal OB development.

scholarly journals Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals

2015 ◽  
Vol 112 (43) ◽  
pp. 13401-13406 ◽  
Author(s):  
Christoph Teufel ◽  
Naresh Subramaniam ◽  
Veronika Dobler ◽  
Jesus Perez ◽  
Johanna Finnemann ◽  
...  
Keyword(s):  
Information Processing ◽  
Prior Knowledge ◽  
Early Psychosis ◽  
Psychotic Symptoms ◽  
Psychotic Experiences ◽  
Healthy Individuals ◽  
Top Down ◽  
Bottom Up ◽  
Psychosis Proneness ◽  
Sensory Evidence

Many neuropsychiatric illnesses are associated with psychosis, i.e., hallucinations (perceptions in the absence of causative stimuli) and delusions (irrational, often bizarre beliefs). Current models of brain function view perception as a combination of two distinct sources of information: bottom-up sensory input and top-down influences from prior knowledge. This framework may explain hallucinations and delusions. Here, we characterized the balance between visual bottom-up and top-down processing in people with early psychosis (study 1) and in psychosis-prone, healthy individuals (study 2) to elucidate the mechanisms that might contribute to the emergence of psychotic experiences. Through a specialized mental-health service, we identified unmedicated individuals who experience early psychotic symptoms but fall below the threshold for a categorical diagnosis. We observed that, in early psychosis, there was a shift in information processing favoring prior knowledge over incoming sensory evidence. In the complementary study, we capitalized on subtle variations in perception and belief in the general population that exhibit graded similarity with psychotic experiences (schizotypy). We observed that the degree of psychosis proneness in healthy individuals, and, specifically, the presence of subtle perceptual alterations, is also associated with stronger reliance on prior knowledge. Although, in the current experimental studies, this shift conferred a performance benefit, under most natural viewing situations, it may provoke anomalous perceptual experiences. Overall, we show that early psychosis and psychosis proneness both entail a basic shift in visual information processing, favoring prior knowledge over incoming sensory evidence. The studies provide complementary insights to a mechanism by which psychotic symptoms may emerge.

scholarly journals Paradoxically sparse chemosensory tuning in broadly-integrating external granule cells in the mouse accessory olfactory bulb

2019 ◽  
Author(s):  
Xingjian Zhang ◽  
Julian P. Meeks
Keyword(s):  
Patch Clamp ◽  
Olfactory Bulb ◽  
Olfactory System ◽  
Granule Cells ◽  
Ex Vivo ◽  
Accessory Olfactory Bulb ◽  
Main Olfactory Bulb ◽  
Patch Clamp Electrophysiology ◽  
Accessory Olfactory System ◽  
Critical Circuit

AbstractThe accessory olfactory bulb (AOB) is a critical circuit in the mouse accessory olfactory system (AOS), but AOB processing is poorly understood compared to the main olfactory bulb (MOB). We used 2-photon GCaMP6f Ca2+ imaging in an ex vivo preparation to study the chemosensory tuning of AOB external granule cells (EGCs), an interneuron population hypothesized to broadly integrate from mitral cells (MCs). We measured MC and EGC tuning to natural chemosignal blends and monomolecular ligands, finding that EGC tuning was far sparser than MC tuning. Simultaneous patch-clamp electrophysiology and Ca2+ imaging indicated that this was only partially explained by lower GCaMP6f-to-spiking ratios in EGCs compared to MCs. Ex vivo patch-clamp recordings revealed that EGC subthreshold responsivity was broad, but monomolecular ligand responses were insufficient to elicit spiking. These results indicate that EGC spiking is selectively engaged by chemosensory blends, suggesting different roles for EGCs than analogous interneurons in the MOB.

scholarly journals Accumulation of sensory evidence is impaired in Parkinson’s disease with visual hallucinations

2017 ◽  
Author(s):  
Claire O’Callaghan ◽  
Julie M. Hall ◽  
Alessandro Tomassini ◽  
Alana J. Muller ◽  
Ishan C. Walpola ◽  
...  
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Sensory Processing ◽  
Sensory Input ◽  
Decision Time ◽  
Visual Hallucinations ◽  
Top Down ◽  
Evidence Accumulation ◽  
Sensory Evidence ◽  
Response Output

AbstractModels of hallucinations across disorders emphasise an imbalance between sensory input and top-down influences over perception. However, the psychological and mechanistic correlates of this imbalance remain underspecified. Visual hallucinations in Parkinson’s disease (PD) are associated with impairments in lower level visual processes and attention, accompanied by over activity and connectivity in higher-order association brain networks. PD therefore provides an attractive framework to explore the relative contributions of bottom-up versus top-down disturbances in hallucinations. Here, we characterised sensory processing in PD patients with and without visual hallucinations, and in healthy controls, by fitting a hierarchical drift diffusion model (hDDM) to an attentional task. The hDDM uses Bayesian estimates to decompose reaction time and response output into parameters reflecting drift rates of evidence accumulation, decision thresholds and non-decision time. We observed slower drift rates in PD patients with hallucinations, which were insensitive to changes in task demand. In contrast, wider decision boundaries and shorter non-decision times relative to controls were found in PD regardless of hallucinator status. Inefficient and less flexible sensory evidence accumulation emerge as unique features of PD hallucinators. We integrate these results with current models of hallucinations, suggesting that slow and inefficient sensory input in PD is less informative, and may therefore be down-weighted leading to an over reliance on top-down influences. Our findings provide a novel computational framework to better specify the impairments in dynamic sensory processing that are a risk factor for visual hallucinations.

scholarly journals Short-Term Plasticity in Cortical GABAergic Synapses on Olfactory Bulb Granule Cells Is Modulated by Endocannabinoids

2021 ◽  
Vol 15 ◽  
Author(s):  
Fu-Wen Zhou ◽  
Adam C. Puche
Keyword(s):  
Olfactory Bulb ◽  
Sensory Processing ◽  
Granule Cell ◽  
Granule Cells ◽  
Cb1 Receptor ◽  
Granule Cell Layer ◽  
Short Term ◽  
Frequency Dependent ◽  
Short Term Plasticity ◽  
Cortical Feedback

Olfactory bulb and higher processing areas are synaptically interconnected, providing rapid regulation of olfactory bulb circuit dynamics and sensory processing. Short-term plasticity changes at any of these synapses could modulate sensory processing and potentially short-term sensory memory. A key olfactory bulb circuit for mediating cortical feedback modulation is granule cells, which are targeted by multiple cortical regions including both glutamatergic excitatory inputs and GABAergic inhibitory inputs. There is robust endocannabinoid modulation of excitatory inputs to granule cells and here we explored whether there was also endocannabinoid modulation of the inhibitory cortical inputs to granule cells. We expressed light-gated cation channel channelrhodopsin-2 (ChR2) in GABAergic neurons in the horizontal limb of the diagonal band of Broca (HDB) and their projections to granule cells in olfactory bulb. Selective optical activation of ChR2 positive axons/terminals generated strong, frequency-dependent short-term depression of GABAA-mediated-IPSC in granule cells. As cannabinoid type 1 (CB1) receptor is heavily expressed in olfactory bulb granule cell layer (GCL) and there is endogenous endocannabinoid release in GCL, we investigated whether activation of CB1 receptor modulated the HDB IPSC and short-term depression at the HDB→granule cell synapse. Activation of the CB1 receptor by the exogenous agonist Win 55,212-2 significantly decreased the peak amplitude of individual IPSC and decreased short-term depression, while blockade of the CB1 receptor by AM 251 slightly increased individual IPSCs and increased short-term depression. Thus, we conclude that there is tonic endocannabinoid activation of the GABAergic projections of the HDB to granule cells, similar to the modulation observed with glutamatergic projections to granule cells. Modulation of inhibitory synaptic currents and frequency-dependent short-term depression could regulate the precise balance of cortical feedback excitation and inhibition of granule cells leading to changes in granule cell mediated inhibition of olfactory bulb output to higher processing areas.

scholarly journals Building Thinking Machines by Solving Animal Cognition Tasks

2020 ◽  
Vol 30 (4) ◽  
pp. 589-615 ◽  
Author(s):  
Matthew Crosby
Keyword(s):  
Predictive Models ◽  
Sensory Input ◽  
Animal Cognition ◽  
Top Down ◽  
Imitation Game ◽  
Bottom Up ◽  
Computing Machinery

AbstractIn ‘Computing Machinery and Intelligence’, Turing, sceptical of the question ‘Can machines think?’, quickly replaces it with an experimentally verifiable test: the imitation game. I suggest that for such a move to be successful the test needs to be relevant, expansive, solvable by exemplars, unpredictable, and lead to actionable research. The Imitation Game is only partially successful in this regard and its reliance on language, whilst insightful for partially solving the problem, has put AI progress on the wrong foot, prescribing a top-down approach for building thinking machines. I argue that to fix shortcomings with modern AI systems a nonverbal operationalisation is required. This is provided by the recent Animal-AI Testbed, which translates animal cognition tests for AI and provides a bottom-up research pathway for building thinking machines that create predictive models of their environment from sensory input.

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