A whole-brain atlas of monosynaptic input targeting four different cell types in the medial prefrontal cortex of the mouse

Ährlund-Richter, Sofie; Xuan, Yang; Lunteren, Josina Anna van; Kim, Hoseok; Ortiz, Cantin; Dorocic, Iskra Pollak; Meletis, Konstantinos; Carlén, Marie

doi:10.1038/s41593-019-0354-y

Cited by 169 publications

(151 citation statements)

References 69 publications

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“…The remaining cortex-projecting GPe neurons were ChAT -, i.e., non-cholinergic. Our results are highly 65 consistent with prior observations (Ahrlund-Richter et al, 2019;Saunders et al, 2015). However, as the identity of non-cholinergic, cortically-projecting neurons remains elusive, we sought to characterize the molecular profile of these neurons.…”

supporting

confidence: 90%

“…projecting GPe neurons (Ahrlund-Richter et al, 2019;Chen et al, 2015;Saunders et al, 2015;Schwarz et al, 2015), CTb was injected into various cortical regions of Dbx1-L-tdTom mice. Systemic analysis of multiple cortical areas including the somatomotor (MO, n = 4 mice), somatosensory (SS, n = 2 mice), anterior cingulate (AC, n = 1 mouse), agranular (AG) and orbital (ORB, n = 2 mice) cortices revealed Dbx1 + neurons do not project to any of these cortical regions (0 out of 52 neurons, 9 sections).…”

Section: Dbx1 + -Pv + Neurons Exhibit Canonical Pv + Neurons Projectimentioning

confidence: 99%

“…In this study, we hypothesize the existence of a unique Lhx6 + GPe population that corresponds to the PVand Npas1 -(PV --Npas1 -) neurons we previously identified and accounts for ~15-20% of the total GPe neuron population (Hernandez et al, 2015). These neurons could play an important role in neural function if they target a unique brain area, such 15 as the cortex, which has been described recently (Ahrlund-Richter et al, 2019;Chen et al, 2015;Saunders et al, 2015;Schwarz et al, 2015). With the advent of additional transgenic lines and viruses, we used molecular marker expression and connectome analysis to reconcile discrepancies and provide a more in-depth analysis of the neuronal makeup and its diversity within the GPe.…”

mentioning

confidence: 99%

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Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Abecassis¹,

Berceau²,

Win³

et al. 2019

Preprint

108

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Within the basal ganglia circuit, the external globus pallidus (GPe) is critically involved in motor control. Aside from Foxp2+ neurons and ChAT+ neurons that have been established as unique neuron types, there is little consensus on the classification of GPe neurons. Properties of the remaining neuron types are poorly-defined. In this study, we leverage new mouse lines, viral tools, and molecular markers to better define GPe neuron subtypes. We found that Sox6 represents a novel, defining marker for GPe neuron subtypes. Lhx6+ neurons that lack the expression of Sox6 were devoid of both parvalbumin and Npas1. This result confirms previous assertions of the existence of a unique Lhx6+ population. Neurons that arise from the Dbx1+ lineage were similarly abundant in the GPe and displayed a heterogeneous makeup. Importantly, tracing experiments revealed that Npas1+-Nkx2.1+ neurons represent the principal non-cholinergic, cortically-projecting neurons. In other words, they form the pallido-cortical arm of the cortico-pallido-cortical loop. Our data further described that pyramidal-tract neurons in the cortex collateralized within the GPe, forming a closed-loop system between the two brain structures. Overall, our findings reconcile some of the discrepancies that arose from differences in techniques or the reliance on pre-existing tools. While spatial distribution and electrophysiological properties of GPe neurons reaffirm the diversification of GPe subtypes, statistical analyses strongly support the notion that these neuron subtypes can be categorized under the two principal neuron classes—i.e., PV+ neurons and Npas1+ neurons.Significance statementThe poor understanding of the neuronal composition in the GPe undermines our ability to interrogate its precise behavioral and disease involvements. In this study, twelve different genetic crosses were used, hundreds of neurons were electrophysiologically-characterized, and over 100,000 neurons were histologically- and/or anatomically-profiled. Our current study further establishes the segregation of GPe neuron classes and illustrates the complexity of GPe neurons in adult mice. Our results support the idea that Npas1+-Nkx2.1+ neurons are a distinct GPe neuron subclass. By providing a detailed analysis of the organization of the cortico-pallidal-cortical projection, our findings establish the cellular and circuit substrates that can be important for motor function and dysfunction.

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supporting

confidence: 90%

Section: Dbx1 + -Pv + Neurons Exhibit Canonical Pv + Neurons Projectimentioning

confidence: 99%

mentioning

confidence: 99%

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Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Abecassis¹,

Berceau²,

Win³

et al. 2019

Preprint

108

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“…Recent whole-brain rabies tracing studies did not reveal differences in thalamic innervation of interneuron subtypes in the PFC (Ährlund-Richter et al, 2019;Sun et al, 2019). In contrast, one of our key findings is that MD preferentially drives VIP+ cells in L1b, while VM drives L1a NDNF+ cells.…”

Section: Discussionmentioning

confidence: 96%

Mediodorsal and ventromedial thalamus engage distinct L1 circuits in the prefrontal cortex

Anastasiades

Collins

Carter

2020

Preprint

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“…However, in contrast to previous studies (e.g. Ährlund-Richter et al, 2019;Wall et al, 2016) rather than using multiple Cre-lines to distinguish subpopulations of, for example, GABAergic cells, we have rather studied excitatory and inhibitory classes more generally, using Cre-Off and Cre-On AAVs in Gad2-Cre mice. Thus, this study has not asked whether subtypes of inhibitory or excitatory cells might be differentially innervated, but whether the two classes receive anatomically segregated distant inputs.…”

Section: Discussionmentioning

confidence: 99%

Excitatory and inhibitory L2/3 neurons in mouse primary visual cortex are balanced in their input connectivity

Brown

Cossell

Margrie

2020

Preprint

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Quantitatively characterising brain-wide connectivity of neural circuits is of vital importance in understanding the function of the mammalian cortex. Here we have designed an analytical approach to examine data from hierarchical segmentation ontologies, and applied it in the comparison of long-range presynaptic connectivity onto excitatory and inhibitory neurons in layer 2/3 (L2/3) of mouse primary visual cortex (V1). We find that long-range connections onto these two general cell classes in L2/3 originate from highly similar brain regions, and in similar proportions, when compared to input to layer 6. These anatomical data suggest that distal information received by excitatory and inhibitory networks is highly homogenous in L2/3.

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A whole-brain atlas of monosynaptic input targeting four different cell types in the medial prefrontal cortex of the mouse

Cited by 169 publications

References 69 publications

Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Mediodorsal and ventromedial thalamus engage distinct L1 circuits in the prefrontal cortex

Excitatory and inhibitory L2/3 neurons in mouse primary visual cortex are balanced in their input connectivity

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A whole-brain atlas of monosynaptic input targeting four different cell types in the medial prefrontal cortex of the mouse

Cited by 169 publications

References 69 publications

Npas1+-Nkx2.1+Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Npas1+-Nkx2.1+Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Mediodorsal and ventromedial thalamus engage distinct L1 circuits in the prefrontal cortex

Excitatory and inhibitory L2/3 neurons in mouse primary visual cortex are balanced in their input connectivity

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Product

Resources

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Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop

Npas1⁺-Nkx2.1⁺Neurons Are an Integral Part of the Cortico-pallido-cortical Loop