FosGFP expression does not capture a sensory learning-related engram in superficial layers of mouse barrel cortex

2021 ◽  
Vol 118 (52) ◽  
pp. e2112212118
Author(s):  
Jiseok Lee ◽  
Joanna Urban-Ciecko ◽  
Eunsol Park ◽  
Mo Zhu ◽  
Stephanie E. Myal ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Sensory Information ◽  
Learning Task ◽  
Early Gene ◽  
Sensory Stimuli ◽  
Association Learning ◽  
Neural Ensembles ◽  
Dependent Learning

Immediate-early gene (IEG) expression has been used to identify small neural ensembles linked to a particular experience, based on the principle that a selective subset of activated neurons will encode specific memories or behavioral responses. The majority of these studies have focused on “engrams” in higher-order brain areas where more abstract or convergent sensory information is represented, such as the hippocampus, prefrontal cortex, or amygdala. In primary sensory cortex, IEG expression can label neurons that are responsive to specific sensory stimuli, but experience-dependent shaping of neural ensembles marked by IEG expression has not been demonstrated. Here, we use a fosGFP transgenic mouse to longitudinally monitor in vivo expression of the activity-dependent gene c-fos in superficial layers (L2/3) of primary somatosensory cortex (S1) during a whisker-dependent learning task. We find that sensory association training does not detectably alter fosGFP expression in L2/3 neurons. Although training broadly enhances thalamocortical synaptic strength in pyramidal neurons, we find that synapses onto fosGFP+ neurons are not selectively increased by training; rather, synaptic strengthening is concentrated in fosGFP− neurons. Taken together, these data indicate that expression of the IEG reporter fosGFP does not facilitate identification of a learning-specific engram in L2/3 in barrel cortex during whisker-dependent sensory association learning.

scholarly journals Loss of Calretinin in L5a impairs the formation of the barrel cortex leading to abnormal whisker-mediated behaviors

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Mingzhao Su ◽  
Junhua Liu ◽  
Baocong Yu ◽  
Kaixing Zhou ◽  
Congli Sun ◽  
...  
Keyword(s):  
Information Integration ◽  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Sensory Information ◽  
Membrane Excitability ◽  
Novelty Preference ◽  
Layer 4 ◽  
Dendritic Complexity ◽  
Cortex System

AbstractThe rodent whisker-barrel cortex system has been established as an ideal model for studying sensory information integration. The barrel cortex consists of barrel and septa columns that receive information input from the lemniscal and paralemniscal pathways, respectively. Layer 5a is involved in both barrel and septa circuits and play a key role in information integration. However, the role of layer 5a in the development of the barrel cortex remains unclear. Previously, we found that calretinin is dynamically expressed in layer 5a. In this study, we analyzed calretinin KO mice and found that the dendritic complexity and length of layer 5a pyramidal neurons were significantly decreased after calretinin ablation. The membrane excitability and excitatory synaptic transmission of layer 5a neurons were increased. Consequently, the organization of the barrels was impaired. Moreover, layer 4 spiny stellate cells were not able to properly gather, leading to abnormal formation of barrel walls as the ratio of barrel/septum size obviously decreased. Calretinin KO mice exhibited deficits in exploratory and whisker-associated tactile behaviors as well as social novelty preference. Our study expands our knowledge of layer 5a pyramidal neurons in the formation of barrel walls and deepens the understanding of the development of the whisker-barrel cortex system.

scholarly journals Loss of Calretinin in L5a Impairs the Formation of the Barrel Cortex Leading to Abnormal Behaviors

2021 ◽  
Author(s):  
Mingzhao Su ◽  
Junhua Liu ◽  
Baocong Yu ◽  
Kaixing Zhou ◽  
Congli Sun ◽  
...  
Keyword(s):  
Information Integration ◽  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Sensory Information ◽  
Membrane Excitability ◽  
Novelty Preference ◽  
Abnormal Behaviors ◽  
Dendritic Complexity ◽  
Cortex System

Abstract The rodent whisker-barrel cortex system has been established as an ideal model for studying sensory information integration. The barrel cortex consists of barrel and septa columns that receive information input from the lemniscal and paralemniscal pathways, respectively. L5a is involved in both barrel and septa circuits and play a key role in information integration. However, the role of L5a in the development of the barrel cortex remains unclear. Previously, we found that Calretinin is dynamically expressed in L5a. In this study, we analyzed Cr KO mice and found that the dendritic complexity and length of L5a pyramidal neurons were significantly decreased after Cr ablation. The membrane excitability and excitatory synaptic transmission of L5a neurons were increased. Consequently, the organization of the barrels was impaired. Moreover, L4 spiny stellate cells were not able to properly gather, leading to abnormal formation of barrel walls as the ratio of barrel/septum size obviously decreased. Cr KO mice exhibited deficits in exploratory and whisker-associated tactile behaviors as well as social novelty preference. Our study expands our knowledge of L5a pyramidal neurons in the formation of barrel walls and deepens the understanding of the development of the whisker-barrel cortex system.

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 Phasic and Tonic Patterns of Locus Coeruleus Output Differentially Modulate Sensory Network Function in the Awake Rat

2011 ◽  
Vol 105 (1) ◽  
pp. 69-87 ◽  
Author(s):  
David M. Devilbiss ◽  
Barry D. Waterhouse
Keyword(s):  
Signal Processing ◽  
Locus Coeruleus ◽  
Somatosensory System ◽  
Sensory Information ◽  
Brain Regions ◽  
Sensory Stimuli ◽  
Network Function ◽  
Neural Ensembles ◽  
Neural Computations ◽  
Awake Rat

Neurons of the nucleus locus coeruleus (LC) discharge with phasic bursts of activity superimposed on highly regular tonic discharge rates. Phasic bursts are elicited by bottom-up input mechanisms involving novel/salient sensory stimuli and top-down decision making processes; whereas tonic rates largely fluctuate according to arousal levels and behavioral states. Although it is generally believed that these two modes of activity differentially modulate information processing in LC targets, the unique role of phasic versus tonic LC output on signal processing in cells, circuits, and neural networks of waking animals is not well understood. In the current study, simultaneous recordings of individual neurons within ventral posterior medial thalamus and barrel field cortex of conscious rats provided evidence that each mode of LC output produces a unique modulatory impact on single neuron responsiveness to sensory-driven synaptic input and representations of sensory information across ensembles of simultaneously recorded cells. Each mode of LC activation specifically modulated the relationship between sensory-stimulus intensity and the subsequent responses of individual neurons and neural ensembles. Overall these results indicate that phasic versus tonic modes of LC discharge exert fundamentally different modulatory effects on target neuronal circuits within the rodent trigeminal somatosensory system. As such, each mode of LC output may differentially influence signal processing as a means of optimizing behaviorally relevant neural computations within this sensory network. Likely the ability of the LC system to differentially regulate neural responses and local circuit operations according to behavioral demands extends to other brain regions including those involved in higher cognitive functions.

Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo

10.1038/4569 ◽  
1999 ◽  
Vol 2 (1) ◽  
pp. 65-73 ◽  
Author(s):  
Karel Svoboda ◽  
Fritjof Helmchen ◽  
Winfried Denk ◽  
David W. Tank
Keyword(s):  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Layer 2

scholarly journals Identification of a developmental switch in information transfer between whisker S1 and S2 cortex in mice

2021 ◽  
Author(s):  
Theofanis Karayannis ◽  
Linbi Cai ◽  
Jenq-Wei Yang ◽  
Shen-Ju Chou ◽  
Chia-Fang Wang ◽  
...  
Keyword(s):  
Information Transfer ◽  
Barrel Cortex ◽  
Wide Field ◽  
Sensory Stimuli ◽  
Knock Out ◽  
Electrophysiological Recordings ◽  
Primary Sensory Cortex ◽  
Animal Navigation ◽  
Knock Out Mice

The whiskers of rodents are a key sensory organ that provides critical tactile information for animal navigation and object exploration throughout life. Previous work has explored the developmental sensory-driven activation of the primary sensory cortex processing whisker information (wS1), also called barrel cortex. This body of work has shown that the barrel cortex is already activated by sensory stimuli during the first post-natal week. However, it is currently unknown when over the course of development these stimuli begin being processed by higher order cortical areas, such as secondary whisker somatosensory area (wS2). Here we investigate for the first time the developmental engagement of wS2 by sensory stimuli and the emergence of cortico-cortical communication from wS1 to wS2. Using in vivo wide-field imaging and electrophysiological recordings in control and conditional knock-out mice we find that wS1 and wS2 are able to process bottom-up information coming from the thalamus already right after birth. We identify that it is only at the end of the first post-natal week that wS1 begins to provide excitation into wS2, a connection which begins to acquire feed-forward inhibition characteristics after the second post-natal week. Therefore, we have uncovered a developmental window during which excitatory versus inhibitory functional connectivity between wS1 and wS2 takes place.

scholarly journals Whisker row deprivation affects the flow of sensory information through rat barrel cortex

2017 ◽  
Vol 117 (1) ◽  
pp. 4-17 ◽  
Author(s):  
Vincent Jacob ◽  
Akinori Mitani ◽  
Taro Toyoizumi ◽  
Kevin Fox
Keyword(s):  
Spontaneous Activity ◽  
Information Content ◽  
Barrel Cortex ◽  
Cortical Plasticity ◽  
Neuronal Response ◽  
Sensory Deprivation ◽  
Sensory Information ◽  
Short Latency ◽  
Characteristic Analysis

Whisker trimming causes substantial reorganization of neuronal response properties in barrel cortex. However, little is known about experience-dependent rerouting of sensory processing following sensory deprivation. To address this, we performed in vivo intracellular recordings from layers 2/3 (L2/3), layer 4 (L4), layer 5 regular-spiking (L5RS), and L5 intrinsically bursting (L5IB) neurons and measured their multiwhisker receptive field at the level of spiking activity, membrane potential, and synaptic conductance before and after sensory deprivation. We used Chernoff information to quantify the “sensory information” contained in the firing patterns of cells in response to spared and deprived whisker stimulation. In the control condition, information for flanking-row and same-row whiskers decreased in the order L4, L2/3, L5IB, L5RS. However, after whisker-row deprivation, spared flanking-row whisker information was reordered to L4, L5RS, L5IB, L2/3. Sensory information from the trimmed whiskers was reduced and delayed in L2/3 and L5IB neurons, whereas sensory information from spared whiskers was increased and advanced in L4 and L5RS neurons. Sensory information from spared whiskers was increased in L5IB neurons without a latency change. L5RS cells exhibited the largest changes in sensory information content through an atypical plasticity combining a significant decrease in spontaneous activity and an increase in a short-latency excitatory conductance. NEW & NOTEWORTHY Sensory cortical plasticity is usually quantified by changes in evoked firing rate. In this study we quantified plasticity by changes in sensory detection performance using Chernoff information and receiver operating characteristic analysis. We found that whisker deprivation causes a change in information flow within the cortical layers and that layer 5 regular-spiking cells, despite showing only a small potentiation of short-latency input, show the greatest increase in information content for the spared input partly by decreasing their spontaneous activity.

scholarly journals HIPPOCAMPAL GLUTAMATE MODULATION DURING MEMORY ENCODING: ASSOCIATION WITH AGE AND SUBFIELD VOLUMES

2019 ◽  
Vol 3 (Supplement_1) ◽  
pp. S840-S841
Author(s):  
Chaitali Anand ◽  
Roya Homayouni ◽  
Qijing Yu ◽  
Sruthi Ramesh ◽  
Dalal Khatib ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Age Differences ◽  
Memory Performance ◽  
Age Groups ◽  
Learning Task ◽  
Resonance Spectroscopy ◽  
Association Learning ◽  
Age Related ◽  
Younger Age

Abstract Hippocampal glutamatergic activity plays a pivotal role in memory consolidation, including the ability to form novel associations that declines with age. To test whether glutamatergic dysfunction may underpin age-related memory declines, we examined in vivo age differences in hippocampal glutamate modulation during encoding of associations, and its relationship with hippocampal subfield volumes. Proton functional magnetic resonance spectroscopy was performed on 32 young (25.1±2.8 years; 18 females) and 16 older (65.9±2.7 years; 7 females) adults to measure changes in hippocampal (randomly assigned right or left) glutamate during an object-location paired association learning task (with 12 cycles of encoding-retrieval epochs). Volumes of the dentate gyrus&CA3, CA1, subiculum, and entorhinal cortex were manually measured from T2-weighted MRI images. Memory performance differed between the age-groups [F(1, 46)=8.56, p<.01], with the older attaining a lower asymptote [t(46)=2.93, p<.05] compared to the younger. Age differences in glutamate were observed only during encoding (age-group x epoch: F(3,137)=5.28, p<.01), and varied over the epochs. Young adults showed increased glutamate during the first four encoding epochs of each cycle, with levels remaining high thereafter. Old adults evidenced a decrease in glutamate during the first four epochs, and a slow, sustained ramping-up afterwards. Including both age-groups, the maximum change in glutamate, calculated using the maximum and minimum levels during encoding, was positively associated with CA1 [F(2,39)=4.28, p<.05] and the dentate gyrus&CA3 volume [F(2,39)=4.4, p<.05], after correcting for multiple comparisons. Glutamate modulation specific to encoding may underlie age-related memory declines and be related to selected hippocampal subfield volumes.

scholarly journals Robustness of sensory-evoked excitation is increased by inhibitory inputs to distal apical tuft dendrites

2015 ◽  
Vol 112 (45) ◽  
pp. 14072-14077 ◽  
Author(s):  
Robert Egger ◽  
Arno C. Schmitt ◽  
Damian J. Wallace ◽  
Bert Sakmann ◽  
Marcel Oberlaender ◽  
...  
Keyword(s):  
Synaptic Input ◽  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Cell Types ◽  
Cortical Layer ◽  
Evoked Responses ◽  
Apical Tuft ◽  
Sensory Evoked ◽  
Pharmacological Manipulations

Cortical inhibitory interneurons (INs) are subdivided into a variety of morphologically and functionally specialized cell types. How the respective specific properties translate into mechanisms that regulate sensory-evoked responses of pyramidal neurons (PNs) remains unknown. Here, we investigated how INs located in cortical layer 1 (L1) of rat barrel cortex affect whisker-evoked responses of L2 PNs. To do so we combined in vivo electrophysiology and morphological reconstructions with computational modeling. We show that whisker-evoked membrane depolarization in L2 PNs arises from highly specialized spatiotemporal synaptic input patterns. Temporally L1 INs and L2–5 PNs provide near synchronous synaptic input. Spatially synaptic contacts from L1 INs target distal apical tuft dendrites, whereas PNs primarily innervate basal and proximal apical dendrites. Simulations of such constrained synaptic input patterns predicted that inactivation of L1 INs increases trial-to-trial variability of whisker-evoked responses in L2 PNs. The in silico predictions were confirmed in vivo by L1-specific pharmacological manipulations. We present a mechanism—consistent with the theory of distal dendritic shunting—that can regulate the robustness of sensory-evoked responses in PNs without affecting response amplitude or latency.

scholarly journals Distinct in vivo dynamics of excitatory synapses onto cortical pyramidal neurons and inhibitory interneurons

2021 ◽  
Author(s):  
Joshua B. Melander ◽  
Aran Nayebi ◽  
Bart C. Jongbloets ◽  
Dale A. Fortin ◽  
Maozhen Qin ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Synaptic Weight ◽  
Barrel Cortex ◽  
Inhibitory Neurons ◽  
Inhibitory Interneurons ◽  
Excitatory Synapses ◽  
Cell Type ◽  
Cortical Function ◽  
Cell Type Specific

SUMMARYCortical function relies on the balanced activation of excitatory and inhibitory neurons. However, little is known about the organization and dynamics of shaft excitatory synapses onto cortical inhibitory interneurons, which cannot be easily identified morphologically. Here, we fluorescently visualize the excitatory postsynaptic marker PSD-95 at endogenous levels as a proxy for excitatory synapses onto layer 2/3 pyramidal neurons and parvalbumin-positive (PV+) inhibitory interneurons in the mouse barrel cortex. Longitudinal in vivo imaging reveals that, while synaptic weights in both neuronal types are log-normally distributed, synapses onto PV+ neurons are less heterogeneous and more stable. Markov-model analyses suggest that the synaptic weight distribution is set intrinsically by ongoing cell type-specific dynamics, and substantial changes are due to accumulated gradual changes. Synaptic weight dynamics are multiplicative, i.e., changes scale with weights, though PV+ synapses also exhibit an additive component. These results reveal that cell type-specific processes govern cortical synaptic strengths and dynamics.

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