Synaptic connectivity between rat striatal spiny projection neurons in vivo: Unexpected multiple somatic innervation in the context of overall sparse proximal connectivity

Oorschot, Dorothy E.; Lin, Naili; Cooper, Benjamin H.; Reynolds, John N. J.; Sun, Huayu; Wickens, Jeffery R.

doi:10.1016/j.baga.2013.04.001

Cited by 14 publications

(22 citation statements)

References 66 publications

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“…We propose that the large number of SPNs and wide distribution of measured synaptic strengths [35,36,84] provide the basis for lateral inhibition to affect striatal output and, consequently, future cortical activity [85]. Striatal inhibitory INs, on the other hand, might influence the functional connectivity of SPNs, thus promoting changes between different states of low correlation in the striatum that might encode specific motor programs.…”

Section: Discussionmentioning

confidence: 99%

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Klaus

Plenz

2016

PLoS Biol

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During quiet resting behavior, involuntary movements are suppressed. Such movement control is attributed to cortico-basal ganglia loops, yet population dynamics within these loops during resting and their relation to involuntary movements are not well characterized. Here, we show by recording cortical and striatal ongoing population activity in awake rats during quiet resting that intrastriatal inhibition maintains a low-correlation striatal resting state in the presence of cortical neuronal avalanches. Involuntary movements arise from disturbed striatal resting activity through two different population dynamics. Nonselectively reducing intrastriatal γ-aminobutyric acid (GABA) receptor-A inhibition synchronizes striatal dynamics, leading to involuntary movements at low rate. In contrast, reducing striatal interneuron (IN)-mediated inhibition maintains decorrelation and induces intermittent involuntary movements at high rate. This latter scenario was highly effective in modulating cortical dynamics at a subsecond timescale. To distinguish intrastriatal processing from loop dynamics, cortex-striatum-midbrain cultures, which lack feedback to cortex, were used. Cortical avalanches in vitro were accompanied by low-correlated resting activity in the striatum and nonselective reduction in striatal inhibition synchronized striatal neurons similar to in vivo. Importantly, reduction of inhibition from striatal INs maintained low correlations in the striatum while reorganizing functional connectivities among striatal neurons. Our results demonstrate the importance of two major striatal microcircuits in distinctly regulating striatal and cortical resting state dynamics. These findings suggest that specific functional connectivities of the striatum that are maintained by local inhibition are important in movement control.

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Section: Discussionmentioning

confidence: 99%

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Klaus

Plenz

2016

PLoS Biol

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“…Analysis of a strain difference between types of midbrain dopamine neurons was made possible by the availability of the animals and associated tissues and was of interest because of previous anatomical and functional studies that we have performed on the basal ganglia of Sprague‐Dawley rats (see, e.g., Galvin and Oorschot, ; Hobbs and Oorschot, ; Kohe, ; Kohe et al, ; Oorschot et al, ) and Wistar rats (Reynolds et al, ; Tunstall et al, ; Sizemore et al, ; Schulz et al, ; Oorschot et al, ).…”

Section: Methodsmentioning

confidence: 99%

“…The sixth rat (rat 6, Wistar) was part of a striatal study in which a spiny projection neuron was injected intracellularly with biocytin during electrophysiological recording in vivo (Oorschot et al, ). This spiny projection neuron's biocytin‐labeled local axons and synapses were traced to other unlabeled postsynaptic spiny projection neurons in an adjacent 50‐µm section (Oorschot et al, ). This adjacent section was used to map the total number of synapses onto the somata and proximal dendrites of three unlabeled spiny projection neurons (i.e., neurons 272, 420, and 558 in Fig.…”

Section: Methodsmentioning

confidence: 99%

Marked differences in the number and type of synapses innervating the somata and primary dendrites of midbrain dopaminergic neurons, striatal cholinergic interneurons, and striatal spiny projection neurons in the rat

Sizemore

Zhang

Lin

et al. 2015

J of Comparative Neurology

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Elucidating the link between cellular activity and goal-directed behavior requires a fuller understanding of the mechanisms underlying burst firing in midbrain dopaminergic neurons and those that suppress activity during aversive or non-rewarding events. We have characterized the afferent synaptic connections onto these neurons in the rat substantia nigra pars compacta (SNpc) and ventral tegmental area (VTA), and compared these findings with cholinergic interneurons and spiny projection neurons in the striatum. We found that the average absolute number of synapses was three to three and one-half times greater onto the somata of dorsal striatal spiny projection neurons than onto the somata of dopaminergic neurons in the SNpc or dorsal striatal cholinergic interneurons. A similar comparison between populations of dopamine neurons revealed a two times greater number of somatic synapses on VTA dopaminergic neurons than SNpc dopaminergic neurons. The percentage of symmetrical, presumably inhibitory, synaptic inputs on somata was significantly higher on spiny projection neurons and cholinergic interneurons compared with SNpc dopaminergic neurons. Synaptic data on the primary dendrites yielded similar significant differences for the percentage of symmetrical synapses for VTA dopaminergic vs. striatal neurons. No differences in the absolute number or type of somatic synapses were evident for dopaminergic neurons in the SNpc of Wistar vs. Sprague-Dawley rat strains. These data from identified neurons are pivotal for interpreting their electrophysiological responses to afferent activity and for generating realistic computer models of neuronal networks of striatal and midbrain dopaminergic function.

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“…Despite the fact that there is no easily visualized pattern of SPN connectivity, several pieces of evidence point to an overall structure: 1) the connection probability is asymmetrical between SPN subclasses where iSPNs are more likely than dSPNs to be connected to both dSPNs and other iSPNs, while dSPNs are more likely to synapse on other dSPNs (Planert et al, 2010; Taverna et al, 2008); 2) the synaptic contacts made by iSPNs produce larger responses than those from dSPNs (Planert et al, 2010; Taverna et al, 2008, 2004; Tunstall et al, 2002); 3) connections are unidirectional in nature and sparse so they do not just contact every nearby SPN (Planert et al, 2010; Taverna et al, 2008, 2004; Tunstall et al, 2002); and 4) SPNs synapse mainly onto distal dendrites of other SPNs, although there is some diversity on location suggesting different types of collateral synapses (Oorschot et al, 2013). These properties suggest a more complex, nonrandom functional organization of lateral inhibition in the striatum.…”

Section: A Conceptual Model Of Synaptic Organization Of the Lateramentioning

confidence: 99%

“…As SPN collaterals synapse mainly on distal dendrites (Oorschot et al, 2013) , and plateau upstate potentials are generated by regenerative events in the distal dendrites (Plotkin et al, 2011), GABA released from SPN could provide sufficient shunting to prevent this transition. Indeed, in vitro studies show that GABA antagonists prolong SPN upstate duration, suggesting that GABA inputs plays a role in upstate timing (Vergara et al, 2003).…”

Section: A Conceptual Model Of Synaptic Organization Of the Lateramentioning

confidence: 99%

Striatal Local Circuitry: A New Framework for Lateral Inhibition

Burke

Rotstein

Alvarez

2017

Neuron

202

209

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This Perspective will examine the organization of intrastriatal circuitry, review recent findings in this area, and discuss how the pattern of connectivity between striatal neurons might give rise to the behaviorally observed synergism between the direct/indirect pathway neurons. The emphasis of this Perspective is on the underappreciated role of lateral inhibition between striatal projection cells in controlling neuronal firing and shaping the output of this circuit. We review some classic studies in combination with more recent anatomical and functional findings to lay out a framework for an updated model of the local intra-striatal circuitry and its contribution to the formation of functional units of processing with the striatum and the integration and filtering of inputs to generate motor patterns and learned behaviors.

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Synaptic connectivity between rat striatal spiny projection neurons in vivo: Unexpected multiple somatic innervation in the context of overall sparse proximal connectivity

Cited by 14 publications

References 66 publications

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Marked differences in the number and type of synapses innervating the somata and primary dendrites of midbrain dopaminergic neurons, striatal cholinergic interneurons, and striatal spiny projection neurons in the rat

Striatal Local Circuitry: A New Framework for Lateral Inhibition

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