Sequentially Switching Cell Assemblies in Random Inhibitory Networks of Spiking Neurons in the Striatum

Ponzi, Adam; Wickens, Jeffery R.

doi:10.1523/jneurosci.5540-09.2010

Cited by 102 publications

(161 citation statements)

References 102 publications

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“…The activity of striatal MSNs and their response to excitatory input, is further modulated by concurrent inhibition derived from collaterals of neighboring MSNs and local interneurons (Tepper and Plenz, 2006;Ponzi and Wickens, 2010). As a first test of the hypothesis that histamine modulates inhibitory input to MSNs we used intrastriatal electrical stimulation, in the presence of blockers of excitatory transmission, to recruit all inhibitory afferents to MSNs simultaneously.…”

Section: Histamine Differentially Modulates Striatal Inhibitionmentioning

confidence: 99%

Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

Ellender¹,

Huerta-Ocampo²,

Deisseroth³

et al. 2011

J. Neurosci.

113

134

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Information processing in the striatum is critical for basal ganglia function and strongly influenced by neuromodulators (e.g., dopamine). The striatum also receives modulatory afferents from the histaminergic neurons in the hypothalamus which exhibit a distinct diurnal rhythm with high activity during wakefulness, and little or no activity during sleep. In view of the fact that the striatum also expresses a high density of histamine receptors, we hypothesized that released histamine will affect striatal function. We studied the role of histamine on striatal microcircuit function by performing whole-cell patch-clamp recordings of neurochemically identified striatal neurons combined with electrical and optogenetic stimulation of striatal afferents in mouse brain slices. Bath applied histamine had many effects on striatal microcircuits. Histamine, acting at H 2 receptors, depolarized both the direct and indirect pathway medium spiny projection neurons (MSNs). Excitatory, glutamatergic input to both classes of MSNs from both the cortex and thalamus was negatively modulated by histamine acting at presynaptic H 3 receptors. The dynamics of thalamostriatal, but not corticostriatal, synapses were modulated by histamine leading to a facilitation of thalamic input. Furthermore, local inhibitory input to both classes of MSNs was negatively modulated by histamine. Subsequent dual whole-cell patch-clamp recordings of connected pairs of striatal neurons revealed that only lateral inhibition between MSNs is negatively modulated, whereas feedforward inhibition from fast-spiking GABAergic interneurons onto MSNs is unaffected by histamine. These findings suggest that the diurnal rhythm of histamine release entrains striatal function which, during wakefulness, is dominated by feedforward inhibition and a suppression of excitatory drive.

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Section: Histamine Differentially Modulates Striatal Inhibitionmentioning

confidence: 99%

Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

Ellender¹,

Huerta-Ocampo²,

Deisseroth³

et al. 2011

J. Neurosci.

113

134

View full text Add to dashboard Cite

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“…However, physiological studies have found these lateral connec- tions to be sparse, weak, and asymmetrical (Jaeger et al, 1994;Tunstall et al, 2002;Koos et al, 2004;Tepper et al, 2004;Planert et al, 2010) thus casting doubt on competitive inhibition as a key computational process in the information processing of the striatum. Ponzi and Wickens (2010) recently showed that in a model based on a realistic striatal inhibitory network, cells form assemblies that fire in sequential coherent episodes. Cell members of the same assembly showed correlated firing rate fluctuations at behaviorally relevant timescales, whereas cell members in different assemblies were negatively correlated.…”

Section: Formation Of Dynamically Changing Functional Correlations Wimentioning

confidence: 99%

Temporal Convergence of Dynamic Cell Assemblies in the Striato-Pallidal Network

Adler¹,

Katabi²,

Finkes³

et al. 2012

J. Neurosci.

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The basal ganglia (BG) have been hypothesized to implement a reinforcement learning algorithm. However, it is not clear how information is processed along this network, thus enabling it to perform its functional role. Here we present three different encoding schemes of visual cues associated with rewarding, neutral, and aversive outcomes by BG neuronal populations.We studied the response profile and dynamical behavior of two populations of projection neurons [striatal medium spiny neurons (MSNs), and neurons in the external segment of the globus pallidus (GPe)], and one neuromodulator group [striatal tonically active neurons (TANs)] from behaving monkeys. MSNs and GPe neurons displayed sustained average activity to cue presentation. The population average response of MSNs was composed of three distinct response groups that were temporally differentiated and fired in serial episodes along the trial. In the GPe, the average sustained response was composed of two response groups that were primarily differentiated by their immediate change in firing rate direction. However, unlike MSNs, neurons in both GPe response groups displayed prolonged and temporally overlapping persistent activity. The putamen TANs stereotyped response was characterized by a single transient response group. Finally, the MSN and GPe response groups reorganized at the outcome epoch, as different task events were reflected in different response groups.Our results strengthen the functional separation between BG neuromodulators and main axis neurons. Furthermore, they reveal dynamically changing cell assemblies in the striatal network of behaving primates. Finally, they support the functional convergence of the MSN response groups onto GPe cells.

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“…It is believed that the striatum integrates these convergent streams of information, with the resulting activity acting on basal ganglia output nuclei connected to association and motor control areas in the cortex (Alexander et al 1986). Computational and experimental studies suggest that the converging input to the striatum leads to the formation of functionally specialized subsets of MSNs with temporally correlated activity patterns (Adler et al 2012;Carrillo-Reid et al 2008;Humphries et al 2009;Ponzi and Wickens 2010;Yim et al 2011). These findings in the striatum, and a large body of work focusing on cortical circuits (Averbeck et al 2006;Bair et al 2001;Cohen and Maunsell 2009;Mitchell et al 2009;Shadlen and Newsome 1998;Zohary et al 1994), implicate correlated activity in neural computation and behavior.…”

mentioning

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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Sequentially Switching Cell Assemblies in Random Inhibitory Networks of Spiking Neurons in the Striatum

Cited by 102 publications

References 102 publications

Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

Temporal Convergence of Dynamic Cell Assemblies in the Striato-Pallidal Network

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

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