scholarly journals Brain state and cortical layer-specific mechanisms underlying perception at threshold

2021 ◽  
Author(s):  
Mitchell P Morton ◽  
Sachira Denagamage ◽  
Isabel J Blume ◽  
John H Reynolds ◽  
Monika P Jadi ◽  
...  
Keyword(s):  
Cortical Layer ◽  
Inhibitory Neurons ◽  
Brain State ◽  
Cortical Layers ◽  
Attention Task ◽  
Sensory Stimuli ◽  
Area V4 ◽  
Perceptual Stability ◽  
Deep Layers ◽  
Perceptual Threshold

Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral readouts despite similarities in sensory input. We hypothesized that fluctuations in neurophysiological states in the sensory neocortex, which could alter cortical processing at the level of neural subpopulations, underlies this perceptual variability. We analyzed cortical layer-specific electrophysiological activity in visual area V4 during a cued attention task. We find that hit trials are characterized by a larger pupil diameter and lower incidence of microsaccades, indicative of a behavioral state with increased arousal and perceptual stability. Target stimuli presented at perceptual threshold evoke elevated multi-unit activity in V4 neurons in hit trials compared to miss trials, across all cortical layers. Putative excitatory and inhibitory neurons are strongly positively modulated in the input (IV) and deep (V & VI) layers of the cortex during hit trials. Excitatory neurons in the superficial cortical layers exhibit lower variability in hit trials. Deep layer neurons are less phase-locked to low frequency rhythms in hits. Hits are also characterized by greater interlaminar coherence between the superficial and deep layers in the pre-stimulus period, and a complementary pattern between the input layer and both the superficial and deep layers in the stimulus-evoked period. Taken together, these results indicate that a state of elevated levels of arousal and perceptual stability allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.

scholarly journals Laminar segregation of sensory coding and behavioral readout in macaque V4

2019 ◽  
Vol 116 (29) ◽  
pp. 14749-14754 ◽  
Author(s):  
Warren W. Pettine ◽  
Nicholas A. Steinmetz ◽  
Tirin Moore
Keyword(s):  
Eye Movements ◽  
Deep Layer ◽  
Visual Stimuli ◽  
Behavioral State ◽  
Visually Guided ◽  
Cortical Layers ◽  
Sensory Stimuli ◽  
Area V4 ◽  
Neuronal Populations ◽  
Deep Layers

Neurons in sensory areas of the neocortex are known to represent information both about sensory stimuli and behavioral state, but how these 2 disparate signals are integrated across cortical layers is poorly understood. To study this issue, we measured the coding of visual stimulus orientation and of behavioral state by neurons within superficial and deep layers of area V4 in monkeys while they covertly attended or prepared eye movements to visual stimuli. We show that whereas single neurons and neuronal populations in the superficial layers conveyed more information about the orientation of visual stimuli than neurons in deep layers, the opposite was true of information about the behavioral relevance of those stimuli. In particular, deep layer neurons encoded greater information about the direction of planned eye movements than superficial neurons. These results suggest a division of labor between cortical layers in the coding of visual input and visually guided behavior.

scholarly journals Demands of visual processing hierarchy shape laminar compartmentalization of attention modulation of luminance contrast in area V4

2021 ◽  
Author(s):  
Xiang Wang ◽  
Anirvan S. Nandy ◽  
Monika P. Jadi
Keyword(s):  
Visual Processing ◽  
Luminance Contrast ◽  
Cortical Layer ◽  
Inhibitory Neurons ◽  
Spatial Integration ◽  
Low Contrast ◽  
Area V4 ◽  
Visual Areas ◽  
Excitatory Neurons ◽  
Contrast Information

ABSTRACTContrast is a key feature of the visual scene that aids object recognition. Attention has been shown to selectively enhance the responses to low contrast stimuli in visual area V4, a critical hub that sends projections both up and down the visual hierarchy. Veridical encoding of contrast information is a key computation in early visual areas, while later stages encode higher level features that benefit from improved sensitivity to low contrast. How area V4 meets these distinct information processing demands in the attentive state is not known. We found that attentional modulation of contrast responses in area V4 is cortical layer and cell-class specific. Putative excitatory neurons in the superficial output layers that project to higher areas show enhanced boosting of low contrast information. On the other hand, putative excitatory neurons of deep output layers that project to early visual areas exhibit contrast-independent scaling. Computational modeling revealed that such layer-wise differences may result from variations in spatial integration extent of inhibitory neurons. These findings reveal that the nature of interactions between attention and contrast in V4 is highly compartmentalized, in alignment with the demands of the visual processing hierarchy.

scholarly journals Laminar Segregation of Sensory Coding and Behavioral Readout in Macaque V4

2018 ◽  
Author(s):  
Warren W. Pettine ◽  
Nicholas A. Steinmetz ◽  
Tirin Moore
Keyword(s):  
Eye Movements ◽  
Deep Layer ◽  
Visual Stimuli ◽  
Behavioral State ◽  
Visually Guided ◽  
Single Neurons ◽  
Sensory Stimuli ◽  
Area V4 ◽  
Neuronal Populations ◽  
Deep Layers

SummaryNeurons in sensory areas of the neocortex are known to represent information both about sensory stimuli and behavioral state, but how these two disparate signals are integrated across cortical layers is poorly understood. To study this issue, we measured the coding of visual stimulus orientation and of behavioral state by neurons within superficial and deep layers of area V4 in monkeys while they covertly attended or prepared eye movements to visual stimuli. We show that single neurons and neuronal populations in superficial layers convey more information about the orientation of visual stimuli, whereas single neurons and neuronal populations in deep layers convey greater information about the behavioral relevance of those stimuli. In particular, deep layer neurons encode greater information about the direction of prepared eye movements. These results reveal a division of labor between laminae in the coding of visual input and visually guided behavior.

scholarly journals Laminar microcircuitry of visual cortex producing attention-associated electric fields

2021 ◽  
Author(s):  
Jacob A. Westerberg ◽  
Michelle S. Schall ◽  
Alexander Maier ◽  
Geoffrey F. Woodman ◽  
Jeffrey D. Schall
Keyword(s):  
Electric Field ◽  
Electric Fields ◽  
Synaptic Activity ◽  
Cortical Layers ◽  
Functional Architecture ◽  
Attention Task ◽  
Area V4 ◽  
Relative Contribution ◽  
Visual Cortical Area ◽  
Prelunate Gyrus

AbstractCognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the component neural circuitry giving rise to these signals remains unknown. Specifically, the functional architecture of cortical columns which results in attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field often measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field capable of being measured extracranially and the relative contribution of each column depends upon the underlying functional architecture.

scholarly journals Statistical Comparison of Spike Responses to Natural Stimuli in Monkey Area V1 With Simulated Responses of a Detailed Laminar Network Model for a Patch of V1

2011 ◽  
Vol 105 (2) ◽  
pp. 757-778 ◽  
Author(s):  
Malte J. Rasch ◽  
Klaus Schuch ◽  
Nikos K. Logothetis ◽  
Wolfgang Maass
Keyword(s):  
Network Model ◽  
Network Models ◽  
Cortical Network ◽  
Inhibitory Neurons ◽  
Sensory Stimuli ◽  
Natural Stimuli ◽  
Cortical Areas ◽  
Model Response ◽  
Spiking Activity

A major goal of computational neuroscience is the creation of computer models for cortical areas whose response to sensory stimuli resembles that of cortical areas in vivo in important aspects. It is seldom considered whether the simulated spiking activity is realistic (in a statistical sense) in response to natural stimuli. Because certain statistical properties of spike responses were suggested to facilitate computations in the cortex, acquiring a realistic firing regimen in cortical network models might be a prerequisite for analyzing their computational functions. We present a characterization and comparison of the statistical response properties of the primary visual cortex (V1) in vivo and in silico in response to natural stimuli. We recorded from multiple electrodes in area V1 of 4 macaque monkeys and developed a large state-of-the-art network model for a 5 × 5-mm patch of V1 composed of 35,000 neurons and 3.9 million synapses that integrates previously published anatomical and physiological details. By quantitative comparison of the model response to the “statistical fingerprint” of responses in vivo, we find that our model for a patch of V1 responds to the same movie in a way which matches the statistical structure of the recorded data surprisingly well. The deviation between the firing regimen of the model and the in vivo data are on the same level as deviations among monkeys and sessions. This suggests that, despite strong simplifications and abstractions of cortical network models, they are nevertheless capable of generating realistic spiking activity. To reach a realistic firing state, it was not only necessary to include both N -methyl-d-aspartate and GABAB synaptic conductances in our model, but also to markedly increase the strength of excitatory synapses onto inhibitory neurons (>2-fold) in comparison to literature values, hinting at the importance to carefully adjust the effect of inhibition for achieving realistic dynamics in current network models.

scholarly journals Functional selectivity and specific connectivity of inhibitory neurons in primary visual cortex

2018 ◽  
Author(s):  
Petr Znamenskiy ◽  
Mean-Hwan Kim ◽  
Dylan R. Muir ◽  
Maria Florencia Iacaruso ◽  
Sonja B. Hofer ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Cells ◽  
Fine Tuning ◽  
Inhibitory Neurons ◽  
Local Network ◽  
Cortical Circuits ◽  
Sensory Stimuli ◽  
Excitatory Neurons ◽  
Strong Excitation

In the cerebral cortex, the interaction of excitatory and inhibitory synaptic inputs shapes the responses of neurons to sensory stimuli, stabilizes network dynamics1 and improves the efficiency and robustness of the neural code2–4. Excitatory neurons receive inhibitory inputs that track excitation5–8. However, how this co-tuning of excitation and inhibition is achieved by cortical circuits is unclear, since inhibitory interneurons are thought to pool the inputs of nearby excitatory cells and provide them with non-specific inhibition proportional to the activity of the local network9–13. Here we show that although parvalbumin-expressing (PV) inhibitory cells in mouse primary visual cortex make connections with the majority of nearby pyramidal cells, the strength of their synaptic connections is structured according to the similarity of the cells’ responses. Individual PV cells strongly inhibit those pyramidal cells that provide them with strong excitation and share their visual selectivity. This fine-tuning of synaptic weights supports co-tuning of inhibitory and excitatory inputs onto individual pyramidal cells despite dense connectivity between inhibitory and excitatory neurons. Our results indicate that individual PV cells are preferentially integrated into subnetworks of inter-connected, co-tuned pyramidal cells, stabilising their recurrent dynamics. Conversely, weak but dense inhibitory connectivity between subnetworks is sufficient to support competition between them, de-correlating their output. We suggest that the history and structure of correlated firing adjusts the weights of both inhibitory and excitatory connections, supporting stable amplification and selective recruitment of cortical subnetworks.

scholarly journals 0074 Inhibitory Neurons in the Dorsomedial Medulla Promote REM Sleep

SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A30-A30
Author(s):  
J Stucynski ◽  
A Schott ◽  
J Baik ◽  
J Hong ◽  
F Weber ◽  
...  
Keyword(s):  
Rem Sleep ◽  
Nrem Sleep ◽  
Inhibitory Neurons ◽  
Brain State ◽  
Sleep Regulation ◽  
Optogenetic Stimulation ◽  
Electrophysiological Recordings ◽  
Stimulation Of

Abstract Introduction The neural circuits controlling rapid eye movement (REM) sleep, and in particular the role of the medulla in regulating this brain state, remains an active area of study. Previous electrophysiological recordings in the dorsomedial medulla (DM) and electrical stimulation experiments suggested an important role of this area in the control of REM sleep. However the identity of the involved neurons and their precise role in REM sleep regulation are still unclear. Methods The properties of DM GAD2 neurons in mice were investigated through stereotaxic injection of CRE-dependent viruses in conjunction with implantation of electrodes for electroencephalogram (EEG) and electromyogram (EMG) recordings and optic fibers. Experiments included in vivo calcium imaging (fiber photometry) across sleep and wake states, optogenetic stimulation of cell bodies, chemogenetic excitation and suppression (DREADDs), and connectivity mapping using viral tracing and optogenetics. Results Imaging the calcium activity of DM GAD2 neurons in vivo indicates that these neurons are most active during REM sleep. Optogenetic stimulation of DM GAD2 neurons reliably triggered transitions into REM sleep from NREM sleep. Consistent with this, chemogenetic activation of DM GAD2 neurons increased the amount of REM sleep while inhibition suppressed its occurrence and enhanced NREM sleep. Anatomical tracing revealed that DM GAD2 neurons project to several areas involved in sleep / wake regulation including the wake-promoting locus coeruleus (LC) and the REM sleep-suppressing ventrolateral periaquaductal gray (vlPAG). Optogenetic activation of axonal projections from DM to LC, and DM to vlPAG was sufficient to induce REM sleep. Conclusion These experiments demonstrate that DM inhibitory neurons expressing GAD2 powerfully promote initiation of REM sleep in mice. These findings further characterize the dorsomedial medulla as a critical structure involved in REM sleep regulation and inform future investigations of the REM sleep circuitry. Support R01 HL149133

scholarly journals Molecular specializations of deep cortical layer analogs in songbirds

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Alexander A. Nevue ◽  
Peter V. Lovell ◽  
Morgan Wirthlin ◽  
Claudio V. Mello
Keyword(s):  
In Situ Hybridization ◽  
Motor Function ◽  
Vocal Learning ◽  
Cortical Layer ◽  
Cortical Layers ◽  
Behavioral Traits ◽  
Molecular Features ◽  
Brain Circuitry ◽  
Learning Circuits

Abstract How the evolution of complex behavioral traits is associated with the emergence of novel brain pathways is largely unknown. Songbirds, like humans, learn vocalizations via tutor imitation and possess a specialized brain circuitry to support this behavior. In a comprehensive in situ hybridization effort, we show that the zebra finch vocal robust nucleus of the arcopallium (RA) shares numerous markers (e.g. SNCA, PVALB) with the adjacent dorsal intermediate arcopallium (AId), an avian analog of mammalian deep cortical layers with involvement in motor function. We also identify markers truly unique to RA and thus likely linked to modulation of vocal motor function (e.g. KCNC1, GABRE), including a subset of the known shared markers between RA and human laryngeal motor cortex (e.g. SLIT1, RTN4R, LINGO1, PLXNC1). The data provide novel insights into molecular features unique to vocal learning circuits, and lend support for the motor theory for vocal learning origin.

scholarly journals Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Janelle MP Pakan ◽  
Scott C Lowe ◽  
Evelyn Dylda ◽  
Sander W Keemink ◽  
Stephen P Currie ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Pyramidal Neurons ◽  
Visual Stimulation ◽  
Inhibitory Neurons ◽  
Behavioral State ◽  
Visual Responses ◽  
Cell Type ◽  
Sensory Stimuli ◽  
Context Dependent

Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.

scholarly journals Frequency preference and attention effects across cortical depths in the human primary auditory cortex

2015 ◽  
Vol 112 (52) ◽  
pp. 16036-16041 ◽  
Author(s):  
Federico De Martino ◽  
Michelle Moerel ◽  
Kamil Ugurbil ◽  
Rainer Goebel ◽  
Essa Yacoub ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Task Demands ◽  
Sound Frequency ◽  
7 Tesla ◽  
Cortical Layers ◽  
Functional Responses ◽  
Feed Forward ◽  
Deep Layers

Columnar arrangements of neurons with similar preference have been suggested as the fundamental processing units of the cerebral cortex. Within these columnar arrangements, feed-forward information enters at middle cortical layers whereas feedback information arrives at superficial and deep layers. This interplay of feed-forward and feedback processing is at the core of perception and behavior. Here we provide in vivo evidence consistent with a columnar organization of the processing of sound frequency in the human auditory cortex. We measure submillimeter functional responses to sound frequency sweeps at high magnetic fields (7 tesla) and show that frequency preference is stable through cortical depth in primary auditory cortex. Furthermore, we demonstrate that—in this highly columnar cortex—task demands sharpen the frequency tuning in superficial cortical layers more than in middle or deep layers. These findings are pivotal to understanding mechanisms of neural information processing and flow during the active perception of sounds.

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