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

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

doi:10.1101/2020.01.08.898817

Cited by 30 publications

(48 citation statements)

References 71 publications

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“…On the other hand, it is rather straightforward 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 (Verhulst, 1976;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), recent studies highlight the existence of cortico-pallido-cortical loops (Saunders et al, 2015;Schwarz et al, 2015;Ahrlund-Richter et al, 2019;Karube et al, 2019;Abecassis et al, 2020;Anastasiades et al, 2020;Clayton et al, 2020), though the precise circuit entities involved have yet to be defined. The direct feedback from Npr3 + (aka Npas1 + -Nkx2.1 + ) neurons to cortical regions (Figure 1c, see also (Abecassis et al, 2020)) argues that the action selection is not simply a top-down command.…”

Section: Gpe Neuron Diversitysupporting

confidence: 70%

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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Section: Gpe Neuron Diversitysupporting

confidence: 70%

Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns

Cherian

Cui

Pamukcu

et al. 2020

Preprint

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“…We found that CCK+ interneurons make robust inhibitory connections onto neighboring pyramidal cells in L5 of IL PFC. Importantly, these connections are much stronger onto PT cells, similar to our previous findings for PV+, SOM+, and NDNF+ interneurons ( Anastasiades et al, 2020 ; Anastasiades et al, 2018 ). Biased inhibition is thus a general property of inhibitory connections in the PFC, although strength also depends on intrinsic properties ( Anastasiades et al, 2018 ).…”

Section: Discussionsupporting

confidence: 89%

“…We found CCK+ inputs are highly restricted to the somatic compartment of both IT and PT cells ( Figure 4—figure supplement 1B & D ). Therefore, in contrast to the strong dendritic innervation by SOM+, 5HT3aR+, and NDNF+ cells ( Anastasiades et al, 2020 ; Marlin and Carter, 2014 ), these results indicate that CCK+ inputs are primarily near the soma of IT and PT cells.…”

Section: Resultsmentioning

confidence: 66%

Hippocampal inputs engage CCK+ interneurons to mediate endocannabinoid-modulated feed-forward inhibition in the prefrontal cortex

Liu

Dimidschstein

Fishell

et al. 2020

eLife

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Connections from the ventral hippocampus (vHPC) to the prefrontal cortex (PFC) regulate cognition, emotion and memory. These functions are also tightly controlled by inhibitory networks in the PFC, whose disruption is thought to contribute to mental health disorders. However, relatively little is known about how the vHPC engages different populations of interneurons in the PFC. Here we use slice physiology and optogenetics to study vHPC-evoked feed-forward inhibition in the mouse PFC. We first show that cholecystokinin (CCK+), parvalbumin (PV+), and somatostatin (SOM+) expressing interneurons are prominent in layer 5 (L5) of infralimbic PFC. We then show that vHPC inputs primarily activate CCK+ and PV+ interneurons, with weaker connections onto SOM+ interneurons. CCK+ interneurons make stronger synapses onto pyramidal tract (PT) cells over nearby intratelencephalic (IT) cells. However, CCK+ inputs undergo depolarization-induced suppression of inhibition (DSI) and CB1 receptor modulation only at IT cells. Moreover, vHPC-evoked feed-forward inhibition undergoes DSI only at IT cells, confirming a central role for CCK+ interneurons. Together, our findings show how vHPC directly engages multiple populations of inhibitory cells in deep layers of the infralimbic PFC, highlighting unexpected roles for both CCK+ interneurons and endocannabinoid modulation in hippocampal-prefrontal communication.

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“…Matrix cells outnumber core cells but are comparatively understudied (Rubio-Garrido et al, 2009). Contrary to their original classification by Lorento de No as “nonspecific” (Lorento de No, 1938), distinct matrix nuclei project to specific cortical regions with sublaminar specificity (Anastasiades et al, 2020; Cruikshank et al, 2012; Yamawaki et al, 2019b). These projections result in subtype-specific activation of cortical inhibitory neuronal subtypes, both in layer 1 (Anastasiades et al, 2020; Cruikshank et al, 2012) and in deeper layers (Delevich et al, 2015), to provide temporally precise regulation of cortical activity (Cruikshank et al, 2012).…”

Section: Introductionmentioning

confidence: 85%

“…Contrary to their original classification by Lorento de No as “nonspecific” (Lorento de No, 1938), distinct matrix nuclei project to specific cortical regions with sublaminar specificity (Anastasiades et al, 2020; Cruikshank et al, 2012; Yamawaki et al, 2019b). These projections result in subtype-specific activation of cortical inhibitory neuronal subtypes, both in layer 1 (Anastasiades et al, 2020; Cruikshank et al, 2012) and in deeper layers (Delevich et al, 2015), to provide temporally precise regulation of cortical activity (Cruikshank et al, 2012). These inputs also target excitatory neurons (Collins et al, 2018; Cruikshank et al, 2012; Guo et al, 2018; Rodriguez-Moreno et al, 2020; Rubio-Garrido et al, 2009; Van Der Werf et al, 2002; Yamawaki et al, 2019b).…”

Section: Introductionmentioning

confidence: 85%

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Brennan

Jedrasiak‐Cape

Kailasa

et al. 2020

Preprint

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The granular retrosplenial cortex (RSG) is critical for both spatial navigation and fear conditioning, but the neural codes enabling these seemingly disparate functions remain unknown. Here, using optogenetic circuit mapping, we reveal a double dissociation that allows parallel circuits in superficial RSG to process navigation- versus fear-related inputs. The anterior thalamus, a source of head direction information, strongly recruits small, low rheobase (LR) pyramidal cells in RSG layer 3. Neighboring regular-spiking (RS) cells are instead preferentially controlled by claustral and anterior cingulate inputs, sources of higher-order and fear-related information. Precise sublaminar axonal and dendritic arborization within RSG layer 1 enable this parallel processing. Synaptic dynamics and computational modeling suggest LR neurons are optimally-tuned conjunctive encoders of direction and distance inputs from the thalamus and dorsal subiculum, respectively. RS cells are better positioned to support contextual fear memories. Thus, parallel input streams to computationally-distinct principal neurons help facilitate diverse RSG functions.

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

Abstract: 150 Introduction: 630 Results: 3,236 Discussion: 1,357 Figures: 8 + 8 supplementary figures + 2 supplementary tables ACKNOWLEDGEMENTSWe thank the Carter lab for helpful discussions and comments on the manuscript. This work was supported by NIH T32 GM007308 (DPC) and NIH R01 MH085974 (AGC).

Cited by 30 publications

References 71 publications

Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns

Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns

Hippocampal inputs engage CCK+ interneurons to mediate endocannabinoid-modulated feed-forward inhibition in the prefrontal cortex

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

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