An Embedded Subnetwork of Highly Active Neurons in the Neocortex

Yassin, Lina; Benedetti, Brett L.; Jouhanneau, Jean-Sébastien; Wen, Jing; Poulet, James F.A.; Barth, Alison L.

doi:10.1016/j.neuron.2010.11.029

Cited by 207 publications

(238 citation statements)

References 47 publications

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“…On one hand, there may be a biological basis for this relationship: for example, experiments in cortical circuits show that highly active cells are more likely to be coupled (Yassin et al 2010). However, to examine whether temporal correlations are purely explained by higher firing, we looked at the relationship between resting firing rate and correlation probability.…”

Section: Mice Learn a Stimulus Discrimination Taskmentioning

confidence: 99%

Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice

Bakhurin

Mac

Golshani

et al. 2016

Journal of Neurophysiology

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Bakhurin KI, Mac V, Golshani P, Masmanidis SC. Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice. J Neurophysiol 115: 1521-1532, 2016. First published January 13, 2016; doi:10.1152/jn.01037.2015.-As the major input to the basal ganglia, the striatum is innervated by a wide range of other areas. Overlapping input from these regions is speculated to influence temporal correlations among striatal ensembles. However, the network dynamics among behaviorally related neural populations in the striatum has not been extensively studied. We used large-scale neural recordings to monitor activity from striatal ensembles in mice undergoing Pavlovian reward conditioning. A subpopulation of putative medium spiny projection neurons (MSNs) was found to discriminate between cues that predicted the delivery of a reward and cues that predicted no specific outcome. These cells were preferentially located in lateral subregions of the striatum. Discriminating MSNs were more spontaneously active and more correlated than their nondiscriminating counterparts. Furthermore, discriminating fast spiking interneurons (FSIs) represented a highly prevalent group in the recordings, which formed a strongly correlated network with discriminating MSNs. Spike time cross-correlation analysis showed the existence of synchronized activity among FSIs and feedforward inhibitory modulation of MSN spiking by FSIs. These findings suggest that populations of functionally specialized (cue-discriminating) striatal neurons have distinct network dynamics that sets them apart from nondiscriminating cells, potentially to facilitate accurate behavioral responding during associative reward learning.

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Section: Mice Learn a Stimulus Discrimination Taskmentioning

confidence: 99%

Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice

Bakhurin

Mac

Golshani

et al. 2016

Journal of Neurophysiology

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“…11 A) of Crym-BAC-EGFP mice and investigated neuronal activity. Because extracellular electrophysiological recording typically has insufficient spatial resolution to discriminate neurons in adjacent repeating units and in vivo Ca 2ϩ imaging is difficult in layer V, we examined activity-induced c-Fos protein expression to investigate neuronal activity (Sagar et al, 1988;Kaczmarek and Chaudhuri, 1997;Farivar et al, 2004;Yassin et al, 2010) (Fig. 11 B, C).…”

Section: Correlated C-fos Expression In Single Repeating Units Under mentioning

confidence: 99%

“…Although c-Fos expression is generally well correlated with neuronal activity (Sagar et al, 1988;Kaczmarek and Chaudhuri, 1997;Farivar et al, 2004;Yassin et al, 2010), it will be necessary in the future to determine how precisely c-Fos expression correlates with action potentials under our experimental conditions. Nevertheless, the correlated c-Fos expression suggests that neurons in single repeating units have similar neuronal activity, and therefore have related functions.…”

Section: Relationship To Previously Characterized Neocortical Structuresmentioning

confidence: 99%

Periodic Organization of a Major Subtype of Pyramidal Neurons in Neocortical Layer V

Maruoka

Kubota²,

Kurokawa³

et al. 2011

J. Neurosci.

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A major question in neocortical research is the extent to which neuronal organization is stereotyped. Previous studies have revealed functional clustering and neuronal interactions among cortical neurons located within tens of micrometers in the tangential orientation (orientation parallel to the pial surface). In the tangential orientation at this scale, however, it is unknown whether the distribution of neuronal subtypes is random or has any stereotypy. We found that the tangential arrangement of subcerebral projection neurons, which are a major pyramidal neuron subtype in mouse layer V, was not random but significantly periodic. This periodicity, which was observed in multiple cortical areas, had a typical wavelength of 30 m. Under specific visual stimulation, neurons in single repeating units exhibited strongly correlated c-Fos expression. Therefore, subcerebral projection neurons have a periodic arrangement, and neuronal activity leading to c-Fos expression is similar among neurons in the same repeating units. These results suggest that the neocortex has a periodic functional micro-organization composed of a major neuronal subtype in layer V.

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“…Despite these findings, it is difficult to predict the overall level of AMPAR function in Arcexpressing neurons, which is influenced by a variety of experience-regulated factors other than Arc. Those factors may promote increases in AMPAR function and counteract Arc's effects (Yassin et al, 2010;Jakkamsetti et al, 2013). In our own experiments, we found that while AMPAR function is altered in HOM mice compared with HET mice, the distribution of AMPAR current levels between GFPϩ and GFPϪ neurons from HET and HOM mice does not correlate with that of persistent firing patterns.…”

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confidence: 99%

Arc Regulates Experience-Dependent Persistent Firing Patterns in Frontal Cortex

Ren

Cao

et al. 2014

J. Neurosci.

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The brain encodes information about past experience in specific populations of neurons that communicate with one another by firing action potentials. Studies of experience-dependent neural plasticity have largely focused on individual synaptic changes in response to neuronal input. Indicative of the neuronal output transmitted to downstream neurons, persistent firing patterns are affected by prior experience in selective neuronal populations. However, little is known about the molecular and cellular mechanisms by which experience-related persistent firing patterns are regulated in specific neuronal populations. Using frontal cortical slices prepared from transgenic mice carrying a fluorescent reporter of Arc gene expression, this study investigates how behavioral experience and the activity-regulated Arc gene affect patterns of neuronal firing. We found that motor training increases Arc expression in subsets of excitatory neurons. Those neurons exhibit persistent firing in contrast to Arc-negative neurons from the same mice or neurons from the untrained mice. Furthermore, in mice carrying genetic deletion of Arc, the frontal cortical circuitry is still in place to initiate experiencedependent gene expression, but the level of persistent firing thereafter is diminished. Finally, our results showed that the emergence of persistent activity is associated with Arc-dependent changes in the function of NMDA-type glutamate receptors, rather than changes in AMPA-type receptors or membrane excitability. Our findings therefore reveal an Arc-dependent molecular pathway by which geneexperience interaction regulates the emergence of persistent firing patterns in specific neuronal populations.

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An Embedded Subnetwork of Highly Active Neurons in the Neocortex

Cited by 207 publications

References 47 publications

Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice

Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice

Periodic Organization of a Major Subtype of Pyramidal Neurons in Neocortical Layer V

Arc Regulates Experience-Dependent Persistent Firing Patterns in Frontal Cortex

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