Mediodorsal and Ventromedial Thalamus Engage Distinct L1 Circuits in the Prefrontal Cortex

Anastasiades, Paul G.; Collins, David P.; Carter, Adam G.

doi:10.1016/j.neuron.2020.10.031

Cited by 100 publications

(99 citation statements)

References 92 publications

(33 reference statements)

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“…However, both experiments used a different strain of modified rabies, SAD-B19G, which has been found to label afferent neurons with a lower efficiency than the CVS-N2cG strain used here (see (Reardon et al, 2016). Thus, our results from both interneurons and projection neurons produce anatomical maps that look substantially different from the existing rabies maps and are more consistent with results provided by traditional retrograde tracers and channelrhodopsin-assisted mapping (CRACM) (Anastasiades et al, 2020;Liu and Carter, 2018).…”

Section: Discussionsupporting

confidence: 76%

“…The cellular targeting of midline thalamic regions to layer 1 NDNF-Cre interneurons, and the corresponding spatial targeting of these axons to the most distal portions of the dendritic arbor of pyramidal cells (Anastasiades et al, 2020), creates a local microcircuit in which feedforward inhibition and feedforward excitation interact directly within the distal apical tuft of pyramidal cells. This motif is consistent with CRACM studies in which mouse frontal cortical NDNF interneurons receive strong and robust input from midline thalamus and control distal dendritic Ca 2+ electrogenesis in frontal cortical pyramidal cells (Anastasiades et al, 2020). The cellular targeting of hippocampal output (e.g., from CA1) to the deeper layers of IL along with interneurons that target the perisomatic (i.e., from PV-Cre neurons) and apical branches (i.e., from SST-Cre neurons) of the pyramidal cell arbor creates a second 'push-pull' microcircuit in the deeper cortical layers.…”

Section: Discussionmentioning

confidence: 99%

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Hippocampal and thalamic afferents form distinct synaptic microcircuits in the mouse frontal cortex

Graham

Spruston

Bloss

2021

Preprint

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Neural circuits within the frontal cortex support the flexible selection of goal-directed behaviors by integrating input from brain regions associated with sensory, emotional, episodic, and semantic memory functions. From a connectomics perspective, determining how these disparate afferent inputs target their synapses to specific cell types in the frontal cortex may prove crucial in understanding circuit-level information processing. Here, we used monosynaptic retrograde rabies mapping to examine the distribution of afferent neurons targeting four distinct classes of local inhibitory interneurons and four distinct classes of excitatory projection neurons in mouse infralimbic cortex. Interneurons expressing parvalbumin, somatostatin, or vasoactive intestinal peptide received a large proportion of inputs from hippocampal regions, while interneurons expressing neuron-derived neurotrophic factor received a large proportion of inputs from thalamic regions. A more moderate hippocampal-thalamic dichotomy was found among the inputs targeting excitatory neurons that project to the basolateral amygdala, lateral entorhinal cortex, nucleus reuniens of the thalamus, and the periaqueductal gray. Together, these results show a prominent bias among hippocampal and thalamic afferent systems in their targeting to genetically or anatomically defined sets of frontal cortical neurons. Moreover, they suggest the presence of two distinct local microcircuits that control how different inputs govern frontal cortical information processing.

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Section: Discussionsupporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Hippocampal and thalamic afferents form distinct synaptic microcircuits in the mouse frontal cortex

Graham

Spruston

Bloss

2021

Preprint

View full text Add to dashboard Cite

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“…On the other hand, it is clear that the inhibitory projection to the STN (and substantial pars reticulata) mediates the motor-promoting effects, and it is consistent with the established relationship between STN activity and movement suppression (Hamani et al, 2004; Aron and Poldrack, 2006; Aron et al, 2007; Eagle et al, 2008; Schmidt et al, 2013; Schweizer et al, 2014; Fife et al, 2017; Wessel and Aron, 2017). In addition to the established literature demonstrating that the GPe sends inhibitory signals to the input and output nuclei of the basal ganglia (Jessell et al, 1978; Mink, 1996; Smith et al, 1998; Kita, 2007; Hegeman et al, 2016; Adam et al, 2020), recent studies highlight the existence of cortico-pallido-cortical loops (Naito and Kita, 1994; Chen et al, 2015; Saunders et al, 2015; Schwarz et al, 2015; Ahrlund-Richter et al, 2019; Karube et al, 2019; Abecassis et al, 2020; Adkins et al, 2020; Anastasiades et al, 2020; Clayton et al, 2020; Gehrlach et al, 2020; Lee et al, 2020; Muñoz-Castañeda et al, 2020; Garcia et al, 2021). However, the precise circuitry has yet to be defined.…”

Section: Discussionmentioning

confidence: 99%

Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns

Cherian

Cui

Pamukcu

et al. 2020

Preprint

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We have previously established that PV+ neurons and Npas1+ neurons are distinct neuron classes in the GPe: they have different topographical, electrophysiological, circuit, and functional properties. Aside from Foxp2+ neurons, which are a unique subclass within the Npas1+ class, we lack driver lines that effectively capture other GPe neuron subclasses. In this study, we examined the utility of Kcng4-Cre, Npr3-Cre, and Npy2r-Cre mouse lines (both males and females) for the delineation of GPe neuron subtypes. By using these novel driver lines, we have provided the most exhaustive investigation of electrophysiological studies of GPe neuron subtypes to date. Corroborating our prior studies, GPe neurons can be divided into two statistically distinct clusters that map onto PV+ and Npas1+ classes. By combining optogenetics,, and machine learning-based tracking, we showed that optogenetic perturbation of GPe neuron subtypes generated unique behavioral structures. Our findings further highlighted the dissociable roles of GPe neurons in regulating movement and anxiety. We concluded that Npr3+ neurons and Kcng4+ neurons are distinct subclasses of Npas1+ neurons and PV+ neurons, respectively. Finally, by examining local collateral connectivity, we inferred the circuit mechanisms involved in the motor patterns observed with optogenetic perturbations. In summary, by identifying mouse lines that allow for manipulations of GPe neuron subtypes, we created new opportunities for interrogations of cellular and circuit substrates that can be important for motor function and dysfunction.

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“…These projections target not only the distal apical dendrites of pyramidal neurons, but also the cINs located within L1 (Ibrahim, Schuman et al 2020). Importantly, the fact that L1 cINs have been shown to receive both thalamic (Ji, Zingg et al 2015) and inter-cortical connections (Leinweber, Ward et al 2017) ideally positions them to modulate incoming sensory inputs and affect excitatory responses (Zhu and Zhu 2004, Jiang, Wang et al 2013, Lee, Wang et al 2015, Anastasiades, Collins et al 2020). L1 cINs have been shown to play a role in, cross-modal integration (Ibrahim, Mesik et al 2016), interhemispheric integration (Palmer, Schulz et al 2012), associative fear learning and plasticity (Abs, Poorthuis et al 2018, Pardi, Vogenstahl et al 2020) as well as sensory motor integration (Mesik, Huang et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Bottom-up inputs are required for the establishment of top-down connectivity onto cortical layer 1 neurogliaform cells

Ibrahim

Huang

Otero

et al. 2021

Preprint

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Higher order feedback projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here, we investigated the contribution of early thalamic inputs onto L1 interneurons for the establishment of top-down inputs in the primary visual cortex. We find that bottom-up thalamic inputs predominate during early L1 development and preferentially target neurogliaform cells. We find that these projections are critical for the subsequent strengthening of feedback inputs from the anterior cingulate cortex. Enucleation or selective removal of thalamic afferents blocked this phenomenon. Notably, while early activation of anterior cingulate afferents resulted in a premature strengthening of these top-down inputs to neurogliaform cells, this was also dependent on thalamic inputs. Our results demonstrate that the proper establishment of top-down feedback inputs critically depends on bottom-up inputs from the thalamus during early postnatal development.

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Mediodorsal and Ventromedial Thalamus Engage Distinct L1 Circuits in the Prefrontal Cortex

Cited by 100 publications

References 92 publications

Hippocampal and thalamic afferents form distinct synaptic microcircuits in the mouse frontal cortex

Hippocampal and thalamic afferents form distinct synaptic microcircuits in the mouse frontal cortex

Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns

Bottom-up inputs are required for the establishment of top-down connectivity onto cortical layer 1 neurogliaform cells

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