scholarly journals Modulation of coordinated activity across cortical layers by plasticity of inhibitory synapses onto layer 5 pyramidal neurons

2019 ◽  
Author(s):  
Joana Lourenço ◽  
Angela Michela De Stasi ◽  
Charlotte Deleuze ◽  
Mathilde Bigot ◽  
Antonio Pazienti ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Information Transfer ◽  
Pyramidal Neurons ◽  
Long Term Potentiation ◽  
Network Activity ◽  
Temporal Association ◽  
Cortical Layers ◽  
Feed Forward ◽  
Sensory Evoked ◽  
Perisomatic Inhibition

AbstractIn the neocortex, synaptic inhibition shapes all forms of spontaneous and sensory-evoked activity. Importantly, inhibitory transmission is highly plastic, but the functional role of inhibitory synaptic plasticity is unknown. In the mouse barrel cortex, activation of layer 2/3 PNs elicited strong feed-forward perisomatic inhibition (FFI) onto layer 5 PNs. We found that FFI involving PV cells was strongly potentiated by postsynaptic PN burst firing. FFI plasticity modified PN excitation-to-inhibition (E/I) ratio, strongly modulated PN gain and altered information transfer across cortical layers. Moreover, our LTPi-inducing protocol modified the firing of layer 5 PNs and altered the temporal association of PN spikes to γ-oscillations both in vitro and in vivo. All these effects were captured by unbalancing the E/I ratio in a feed-forward inhibition circuit model. Altogether, our results indicate that activity-dependent modulation of perisomatic inhibitory strength effectively influences the participation of single principal cortical neurons to cognitive-relevant network activity.Impact StatementLong-term potentiation of feed-forward perisomatic inhibition effectively alters the computational properties of single layer 5 pyramidal neurons and their association to network activity.

scholarly journals GluA4 subunit of AMPA receptors mediates the early synaptic response to altered network activity in the developing hippocampus

2016 ◽  
Vol 115 (6) ◽  
pp. 2989-2996 ◽  
Author(s):  
J. Huupponen ◽  
T. Atanasova ◽  
T. Taira ◽  
S. E. Lauri
Keyword(s):  
Ampa Receptors ◽  
Pyramidal Neurons ◽  
Activity Patterns ◽  
Critical Role ◽  
Long Term Potentiation ◽  
Postnatal Period ◽  
Homeostatic Plasticity ◽  
Network Activity ◽  
Hippocampal Pyramidal Neurons ◽  
Activity Dependent

Development of the neuronal circuitry involves both Hebbian and homeostatic plasticity mechanisms that orchestrate activity-dependent refinement of the synaptic connectivity. AMPA receptor subunit GluA4 is expressed in hippocampal pyramidal neurons during early postnatal period and is critical for neonatal long-term potentiation; however, its role in homeostatic plasticity is unknown. Here we show that GluA4-dependent plasticity mechanisms allow immature synapses to promptly respond to alterations in network activity. In the neonatal CA3, the threshold for homeostatic plasticity is low, and a 15-h activity blockage with tetrodotoxin triggers homeostatic upregulation of glutamatergic transmission. On the other hand, attenuation of the correlated high-frequency bursting in the CA3-CA1 circuitry leads to weakening of AMPA transmission in CA1, thus reflecting a critical role for Hebbian synapse induction in the developing CA3-CA1. Both of these developmentally restricted forms of plasticity were absent in GluA4 −/− mice. These data suggest that GluA4 enables efficient homeostatic upscaling and responsiveness to temporal activity patterns during the critical period of activity-dependent refinement of the circuitry.

scholarly journals Large and fast human pyramidal neurons associate with intelligence

2018 ◽  
Author(s):  
Natalia A. Goriounova ◽  
Djai B. Heyer ◽  
René Wilbers ◽  
Matthijs B. Verhoog ◽  
Michele Giugliano ◽  
...  
Keyword(s):  
Action Potential ◽  
Brain Imaging ◽  
Cortical Thickness ◽  
Cortical Neurons ◽  
Information Transfer ◽  
Pyramidal Neurons ◽  
Temporal Cortex ◽  
Neuron Activity ◽  
Human Intelligence ◽  
Iq Scores

AbstractIt is generally assumed that human intelligence relies on efficient processing by neurons in our brain. Behavioral and brain-imaging studies robustly show that higher intelligence associates with faster reaction times and thicker gray matter in temporal and frontal cortical areas. However, no direct evidence exists that links individual neuron activity and structure to human intelligence. Since a large part of cortical grey matter consists of dendrites, these structures likely determine cortical architecture. In addition, dendrites strongly affect functional properties of neurons, including action potential speed. Thereby, dendritic size and action potential firing may constitute variation in cortical thickness, processing speed, and ultimately IQ.To investigate this, we took advantage of brain tissue available from neurosurgery and recorded from pyramidal neurons in the medial temporal cortex, an area showing high association between cortical thickness, cortical activity and intelligence. Next, we reconstructed full dendritic structures of recorded neurons and combined these with brain-imaging data and IQ scores from the same subjects. We find that high IQ scores and large temporal cortical thickness associate with larger, more complex dendrites of human pyramidal neurons. We show in silico that larger dendrites enable pyramidal neurons to track activity of synaptic inputs with higher temporal precision, due to fast action potential initiation. Finally, we find that human pyramidal neurons of individuals with higher IQ scores sustain faster action potentials during repeated firing. These findings provide first evidence that human intelligence is associated with neuronal complexity, action potential speed and efficient information transfer in cortical neurons.

scholarly journals Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in a three-layer cortex

2016 ◽  
Author(s):  
Nathaniel C. Wright ◽  
Ralf Wessel
Keyword(s):  
Membrane Potential ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Ex Vivo ◽  
Network Activity ◽  
Visual Responses ◽  
Cortical Function ◽  
Sensory Evoked ◽  
High Conductance

A primary goal of systems neuroscience is to understand cortical function, which typically involves studying spontaneous and sensory-evoked cortical activity. Mounting evidence suggests a strong and complex relationship between the ongoing and evoked state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope; it records the activities of a minority of neurons, and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but are difficult to obtain in vivo. Here, we record subthreshold cortical visual responses in the ex vivo turtle eye-attached whole-brain preparation, which is ideally-suited to such a study. In the absence of visual stimulation, the network is “synchronous”; neurons display network-mediated transitions between low- and high-conductance membrane potential states. The prevalence of these slow-wave transitions varies across turtles and recording sessions. Visual stimulation evokes similar high-conductance states, which are on average larger and less reliable when the ongoing state is more synchronous. Responses are muted when immediately preceded by large, spontaneous high-conductance events. Evoked spiking is sparse, highly variable across trials, and mediated by concerted synaptic inputs that are in general only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons.

scholarly journals Rapid Temporal Modulation of Synchrony by Competition in Cortical Interneuron Networks

2004 ◽  
Vol 16 (2) ◽  
pp. 251-275 ◽  
Author(s):  
P.H.E. Tiesinga ◽  
T. J. Sejnowski
Keyword(s):  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Background Activity ◽  
Pyramidal Cells ◽  
Spike Timing ◽  
Network Activity ◽  
Local Networks ◽  
Rapid Changes ◽  
Asynchronous State ◽  
The Impact

The synchrony of neurons in extrastriate visual cortex is modulated by selective attention even when there are only small changes in firing rate (Fries, Reynolds, Rorie, & Desimone, 2001). We used Hodgkin-Huxley type models of cortical neurons to investigate the mechanism by which the degree of synchrony can be modulated independently of changes in firing rates. The synchrony of local networks of model cortical interneurons interacting through GABAA synapses was modulated on a fast timescale by selectively activating a fraction of the interneurons. The activated interneurons became rapidly synchronized and suppressed the activity of the other neurons in the network but only if the network was in a restricted range of balanced synaptic background activity. During stronger background activity, the network did not synchronize, and for weaker background activity, the network synchronized but did not return to an asynchronous state after synchronizing. The inhibitory output of the network blocked the activity of pyramidal neurons during asynchronous network activity, and during synchronous network activity, it enhanced the impact of the stimulus-related activity of pyramidal cells on receiving cortical areas (Salinas & Sejnowski, 2001). Synchrony by competition provides a mechanism for controlling synchrony with minor alterations in rate, which could be useful for information processing. Because traditional methods such as cross-correlation and the spike field coherence require several hundred milliseconds of recordings and cannot measure rapid changes in the degree of synchrony, we introduced a new method to detect rapid changes in the degree of coincidence and precision of spike timing.

scholarly journals Large and fast human pyramidal neurons associate with intelligence

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Natalia A Goriounova ◽  
Djai B Heyer ◽  
René Wilbers ◽  
Matthijs B Verhoog ◽  
Michele Giugliano ◽  
...  
Keyword(s):  
Action Potential ◽  
Cortical Neurons ◽  
Information Transfer ◽  
Pyramidal Neurons ◽  
Human Intelligence ◽  
Temporal Precision ◽  
Physiological Properties ◽  
Efficient Information ◽  
Efficient Processing ◽  
Iq Scores

It is generally assumed that human intelligence relies on efficient processing by neurons in our brain. Although grey matter thickness and activity of temporal and frontal cortical areas correlate with IQ scores, no direct evidence exists that links structural and physiological properties of neurons to human intelligence. Here, we find that high IQ scores and large temporal cortical thickness associate with larger, more complex dendrites of human pyramidal neurons. We show in silico that larger dendritic trees enable pyramidal neurons to track activity of synaptic inputs with higher temporal precision, due to fast action potential kinetics. Indeed, we find that human pyramidal neurons of individuals with higher IQ scores sustain fast action potential kinetics during repeated firing. These findings provide the first evidence that human intelligence is associated with neuronal complexity, action potential kinetics and efficient information transfer from inputs to output within cortical neurons.

scholarly journals Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in the three-layer turtle cortex

2017 ◽  
Vol 118 (4) ◽  
pp. 2142-2155 ◽  
Author(s):  
Nathaniel C. Wright ◽  
Ralf Wessel
Keyword(s):  
Membrane Potential ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Cortical Activity ◽  
Network Activity ◽  
Visual Responses ◽  
Up States ◽  
Evoked Activity ◽  
Sensory Evoked

A primary goal of systems neuroscience is to understand cortical function, typically by studying spontaneous and stimulus-modulated cortical activity. Mounting evidence suggests a strong and complex relationship exists between the ongoing and stimulus-modulated cortical state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope: it records the activity of a minority of neurons and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but stable recordings are difficult to obtain in vivo. Here, we recorded subthreshold cortical visual responses in the ex vivo turtle eye-attached whole brain preparation, which is ideally suited for such a study. We found that, in the absence of visual stimulation, the network was “synchronous”; neurons displayed network-mediated transitions between hyperpolarized (Down) and depolarized (Up) membrane potential states. The prevalence of these slow-wave transitions varied across turtles and recording sessions. Visual stimulation evoked similar Up states, which were on average larger and less reliable when the ongoing state was more synchronous. Responses were muted when immediately preceded by large, spontaneous Up states. Evoked spiking was sparse, highly variable across trials, and mediated by concerted synaptic inputs that were, in general, only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons. NEW & NOTEWORTHY Most studies of cortical activity focus on spikes. Subthreshold membrane potential recordings can provide complementary insight, but stable recordings are difficult to obtain in vivo. Here, we recorded the membrane potentials of cortical neurons during ongoing and visually evoked activity. We observed a strong relationship between network and single-neuron evoked activity spanning multiple temporal scales. The membrane potential perspective of cortical dynamics thus highlights the influence of intrinsic network properties on visual processing.

scholarly journals Emerging feed-forward inhibition allows the robust formation of direction selectivity in the developing ferret visual cortex

2014 ◽  
Vol 111 (11) ◽  
pp. 2355-2373 ◽  
Author(s):  
Stephen D. Van Hooser ◽  
Gina M. Escobar ◽  
Arianna Maffei ◽  
Paul Miller
Keyword(s):  
Visual Cortex ◽  
Cortical Neurons ◽  
Initial Conditions ◽  
Receptive Fields ◽  
Long Term Potentiation ◽  
Direction Selectivity ◽  
Feed Forward ◽  
Synaptic Competition ◽  
Eye Opening ◽  
Feed Forward Inhibition

The computation of direction selectivity requires that a cell respond to joint spatial and temporal characteristics of the stimulus that cannot be separated into independent components. Direction selectivity in ferret visual cortex is not present at the time of eye opening but instead develops in the days and weeks following eye opening in a process that requires visual experience with moving stimuli. Classic Hebbian or spike timing-dependent modification of excitatory feed-forward synaptic inputs is unable to produce direction-selective cells from unselective or weakly directionally biased initial conditions because inputs eventually grow so strong that they can independently drive cortical neurons, violating the joint spatial-temporal activation requirement. Furthermore, without some form of synaptic competition, cells cannot develop direction selectivity in response to training with bidirectional stimulation, as cells in ferret visual cortex do. We show that imposing a maximum lateral geniculate nucleus (LGN)-to-cortex synaptic weight allows neurons to develop direction-selective responses that maintain the requirement for joint spatial and temporal activation. We demonstrate that a novel form of inhibitory plasticity, postsynaptic activity-dependent long-term potentiation of inhibition (POSD-LTPi), which operates in the developing cortex at the time of eye opening, can provide synaptic competition and enables robust development of direction-selective receptive fields with unidirectional or bidirectional stimulation. We propose a general model of the development of spatiotemporal receptive fields that consists of two phases: an experience-independent establishment of initial biases, followed by an experience-dependent amplification or modification of these biases via correlation-based plasticity of excitatory inputs that compete against gradually increasing feed-forward inhibition.

scholarly journals Aη-α and Aη-β peptides impair LTP ex vivo within the low nanomolar range and impact neuronal activity in vivo

2021 ◽  
Vol 13 (1) ◽  
Author(s):  
Maria Mensch ◽  
Jade Dunot ◽  
Sandy M. Yishan ◽  
Samuel S. Harris ◽  
Aline Blistein ◽  
...  
Keyword(s):  
Neuronal Activity ◽  
Ex Vivo ◽  
Long Term Potentiation ◽  
Network Activity ◽  
Strongly Correlated ◽  
App Processing ◽  
Term Potentiation ◽  
Hippocampal Network

Abstract Background Amyloid precursor protein (APP) processing is central to Alzheimer’s disease (AD) etiology. As early cognitive alterations in AD are strongly correlated to abnormal information processing due to increasing synaptic impairment, it is crucial to characterize how peptides generated through APP cleavage modulate synapse function. We previously described a novel APP processing pathway producing η-secretase-derived peptides (Aη) and revealed that Aη–α, the longest form of Aη produced by η-secretase and α-secretase cleavage, impaired hippocampal long-term potentiation (LTP) ex vivo and neuronal activity in vivo. Methods With the intention of going beyond this initial observation, we performed a comprehensive analysis to further characterize the effects of both Aη-α and the shorter Aη-β peptide on hippocampus function using ex vivo field electrophysiology, in vivo multiphoton calcium imaging, and in vivo electrophysiology. Results We demonstrate that both synthetic peptides acutely impair LTP at low nanomolar concentrations ex vivo and reveal the N-terminus to be a primary site of activity. We further show that Aη-β, like Aη–α, inhibits neuronal activity in vivo and provide confirmation of LTP impairment by Aη–α in vivo. Conclusions These results provide novel insights into the functional role of the recently discovered η-secretase-derived products and suggest that Aη peptides represent important, pathophysiologically relevant, modulators of hippocampal network activity, with profound implications for APP-targeting therapeutic strategies in AD.

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