Activation of Direct and Indirect Pathway Medium Spiny Neurons Drives Distinct Brain-wide Responses

Lee, Hyun Joo; Weitz, Andrew J.; Bernal-Casas, David; Duffy, Ben A.; Choy, Michael; Kravitz, Alexxai V.; Kreitzer, Anatol C.; Lee, Jin Hyung

doi:10.1016/j.neuron.2016.06.010

Cited by 108 publications

(127 citation statements)

References 69 publications

(109 reference statements)

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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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“…In small animal fMRI studies, variations in the temporal dynamics of the hemodynamic responses can be more severe than those in human studies. This is likely due to the use of anesthesia to minimize motion and restraint stress (Schlegel et al, 2015; Schroeter et al, 2014; Williams et al, 2010), the use of disease models (Nersesyan et al, 2004; Weber et al, 2008), and the use of direct brain stimulation (Angenstein et al, 2009; Byers et al, 2015; Duffy et al., 2015; Ferenczi et al, 2016; Lee et al, 2016; Lee et al, 2010; Liu et al, 2015; Weitz et al, 2014) in small animal studies. Under these conditions, evoked BOLD responses can differ considerably from the canonical response.…”

Section: Discussionmentioning

confidence: 99%

“…During ofMRI experiments, stray light and local tissue heating associated with the optical stimulation can introduce undesirable artifacts to the data (Christie et al, 2013; Schmid et al, 2016), hence it is important to identify contaminated data during the analysis process. Specifically, artifacts caused by stray light are typically detected in vision-related brain regions (Schmid et al, 2016), whereas optogenetically-evoked responses are usually absent there when the stimulation target is outside of the visual pathway (Byers et al, 2015; Desai et al., 2011; Duffy et al, 2015; Lee et al, 2016; Lee et al, 2010; Liu et al, 2015; Takata et al, 2015; Weitz et al, 2014). As a result, accurate detection of BOLD responses in vision-related regions is essential to identify data contaminated with these artifacts.…”

Section: Discussionmentioning

confidence: 99%

“…ofMRI is a novel technique that combines optogenetics with fMRI readouts (Abe et al, 2012; Desai et al, 2011; Kahn et al, 2013; Lee et al., 2016; Lee et al, 2010; Weitz and Lee, 2013). Compared to conventional electrical stimulation or sensory stimulation, ofMRI allows visualization of the causal effects of specific neuronal populations.…”

Section: Methodsmentioning

confidence: 99%

“…It directly stimulates neurons, which eliminates the confounding effects of stimulating many cell types at the same time. The high level of variability in the evoked BOLD responses reported in recent ofMRI studies (Byers et al, 2015; Desai et al, 2011; Duffy et al, 2015; Lee et al, 2016; Lee et al, 2010; Liu et al, 2015; Takata et al, 2015; Weitz et al, 2014) offers an excellent opportunity to assess the robustness of different methods to cope with heterogeneous BOLD responses.…”

Section: Methodsmentioning

confidence: 99%

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Comparison of fMRI analysis methods for heterogeneous BOLD responses in block design studies

et al. 2017

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A large number of fMRI studies have shown that the temporal dynamics of evoked BOLD responses can be highly heterogeneous. Failing to model heterogeneous responses in statistical analysis can lead to significant errors in signal detection and characterization and alter the neurobiological interpretation. However, to date it is not clear that, out of a large number of options, which methods are robust against variability in the temporal dynamics of BOLD responses in block-design studies. Here, we used rodent optogenetic fMRI data with heterogeneous BOLD responses and simulations guided by experimental data as a means to investigate different analysis methods’ performance against heterogeneous BOLD responses. Evaluations are carried out within the general linear model (GLM) framework and consist of standard basis sets as well as independent component analysis (ICA). Analyses show that, in the presence of heterogeneous BOLD responses, conventionally used GLM with a canonical basis set leads to considerable errors in the detection and characterization of BOLD responses. Our results suggest that the 3rd and 4th order gamma basis sets, the 7th to 9th order finite impulse response (FIR) basis sets, the 5th to 9th order B-spline basis sets, and the 2nd to 5th order Fourier basis sets are optimal for good balance between detection and characterization, while the 1st order Fourier basis set (coherence analysis) used in our earlier studies show good detection capability. ICA has mostly good detection and characterization capabilities, but detects a large volume of spurious activation with the control fMRI data.

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A model for transforming egocentric views into goal‐directed behavior

LaChance

Taube

2023

Hippocampus

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Neurons in the rat postrhinal cortex (POR) respond to the egocentric (observer‐centered) bearing and distance of the boundaries, or geometric center, of an enclosed space. Understanding of the precise geometric and sensory properties of the environment that generate these signals is limited. Here we model how this signal may relate to visual perception of motion parallax along environmental boundaries. A behavioral extension of this tuning is the known ‘centering response’, in which animals follow a spatial gradient function based on boundary parallax to guide behavior toward the center of a corridor or enclosure. Adding an allocentric head direction signal to this representation can translate the gradient across two‐dimensional space and provide a new gradient for directing behavior to any location. We propose a model for how this signal may support goal‐directed navigation via projections to the dorsomedial striatum. The result is a straightforward code for navigational variables derived from visual geometric properties of the surrounding environment, which may be used to map space and transform incoming sensory information into an appropriate motor output.

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Activation of Direct and Indirect Pathway Medium Spiny Neurons Drives Distinct Brain-wide Responses

Cited by 108 publications

References 69 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

Comparison of fMRI analysis methods for heterogeneous BOLD responses in block design studies

A model for transforming egocentric views into goal‐directed behavior

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